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Kollen et al. reviewed 735 available published (clinical) stroke rehabilitation trials [2]. They concluded that conventional treatment approaches induce improvements that are confined to impairment level only and do not generalize at a functional improvement level. In contrast, they stated that the treatment strategies that incorporate a strong emphasis on functional training may hold the key to optimal stroke rehabilitation and that appropriate intensity and task-specific exercise therapy are important components of such an approach. This was later reconfirmed to various degrees by others [3, 4].
Several commercially available devices have been built to deliver repetitive movements to an impaired human hand for stroke survivors to regain the use of the hand. However, the dysfunction of the natural afferent feedback pathways and proprioception hampers the sensory learning process of the patient and its conversion to execution of movement. This contributes to an inadequate restoration of functionality despite reducing impairment at a gross motor level [4, 5]. External manifestations of movement such as trajectory, force, acceleration, range of motion and the like are ultimately dependent on adequate, appropriate, and timely self-regulation of brain and muscle activity specific to various tasks. After an event such as stroke, various compensatory strategies come into play to execute the same movements, which, left unaddressed, become learned behavior. Re-engaging the human being’s innate sensory learning mechanisms to regain the appropriate muscle and neural strategies is, therefore, a challenge and an unmet need. If high repetition-based rehabilitation is embarked upon without such re-learning, one runs the risk of post-trauma compensatory strategies being unknowingly reinforced in the brain, thus restoring movement and function in only a limited manner [6, 7].
The body learns coordination for task performance by using all the lessons learnt from neuro-muscular, inter-limb, intra-limb, and eye-hand co-ordination [8, 9]. The specific strategies used are not only different from task to task for a person, but also differ for any one task between persons [10]. Initially, it was thought that the muscle synergies eliminated the redundant degrees of freedom by constraining the movements of certain joints or muscle [10]. But this does not work very well with the initial pathological constraints of an impaired arm. It has also been shown that constraining the movement of certain joints and muscles requires more energy and neural commands, and hence increases the number of neural signals required to perform the task [11]. However, some strategies are fundamental to all movement, such as maintaining an agonist-antagonist balance in the appropriate muscle groups, a moderation of effort to make repetitions possible during rehabilitation without being confounded by fatigue, and an active brain state which allows one to bring attention to the task at hand in a consistent manner. Facilitating such general strategies with technology rather than directly and artificially controlling individual, task-specific strategies is less complex, requires lower computational power and could facilitate a generalization of such useful strategies to other activities. This could in turn result in higher degrees of independence.
As an illustration, let us consider how humans learn handwriting. This is usually done by tracing over an existing alphabet or joining dots in the shape of an alphabet. Here, constraints are mind imposed based on visual cues while no constraints are placed physically on the hand. These mind-imposed constraints involve seeing a pattern and responding with a pencil, like a sort of static imitation. Everyone may choose a different strategy to impose these constraints, based on the kinematics of the more proximal joints and natural synergies of muscles proximal to the point where control is desired. This is like the uncontrolled manifold hypothesis for motor learning and involves a mechanism by which brain and body complement each other in real-time in managing elemental and contextual variables [12]. Hence, there does seem to be some convergence between motor learning theory and how developmental biology describes babies and infants learning in an associative, Hebbian manner using their sensory and motor faculties. The next question is whether such learning can be used as a pathway to undo the maladaptive, compensatory brain-muscle strategies that are common among chronic stroke patients with upper arm disability and help re-educate the adoption of appropriate strategies.
Stroke is an injury that affects not only body but also cognition and cardiovascular health, among others. Hence, it resembles a systemic injury or trauma even in mild to moderate cases. Healing of such systemic injuries has the final pathway of self-management or self-regulation [13, 14]. Self-regulation is ingrained by a biological, natural model of learning driven by the feedback and feedforward of information [13]. Self-regulation essentially requires a measure (absolute or relative), some facility to monitor changes in real-time, and some training to help develop the skill to modify the measure and move it in a desired direction [14, 15]. In the area of motor recovery, similar benefits of “self-control” have been demonstrated [16] but it is not very clear whether it can result in improvement in functional tasks.
Exercise is one way of providing an enriched motor environment. It facilitates plasticity in the brain and protects against the erosive effects, and this is one of the fundamental principles of early mobilization and continuing long term therapy. However, not all exercise regimens are adaptive, and some may even be maladaptive. In animal studies, the location and type of injury appear to dictate to some extent whether the intensity of motor rehabilitation training results in pro-plasticity, neutral or adverse contralesional hemisphere effects [17]. Additionally, the contralesional hemisphere appears to benefit from early, intense, motor enrichment while the perilesional area may be most helped by a gradual, modest increase in therapy. On another note, if the motivation to use the impaired limb after stroke is reduced due to ineptitude, pain or fatigue in that limb and there is a corresponding increased reliance on the other extremity, “learned non-use” of the impaired limb is the result [18].
While remarkable improvements in function have been reported when the non-impaired arm is constrained, as in constraint-induced therapy [19], excessively intense therapy can also lead to increased chances of secondary tissue loss due to reduction of brain derived neurotrophic factor (BDNF) expression in the brain during recovery [20]. Thus, while early onset of therapy using repetitive practice is vital to recovery, too much of it can exaggerate the extent of injury. This becomes even more significant because commonly used clinical assessment tests are not sensitive to small changes and do not allow the experimenter to distinguish between actual neurological recovery and behavioral compensation [21]. Just as neuroplasticity is a mechanism which can be leveraged to regain function, training of inappropriate, compensatory muscle and neural strategies, adopted unknowingly, can just as easily get ingrained in the brain and may take a long time to undo. The chances of this happening are heightened after stroke, when touch function, proprioception and cognition are adversely affected, and self-regulation ability is reduced due to the disruption of the natural feedback loops. Hence, apart from re-learning brain and muscle strategies, self-regulation of intensity in order to consistently keep compensation at bay and maintain beneficial strategies during training is another important component in this learning-led recovery model.
Like in the handwriting example given earlier, any learning model must satisfy the requirements of an experience derived from a sensory-rich system, as well as a motor system free of artificial constraints, which can adequately choose the synergy and/or strategy necessary to respond to this sensory system [22]. This is very similar to infants who learn in a non-instructional manner rich in sensory experience, using a feedforward-feedback sampling process [23]. Like in infants, the presence of such plasticity may provide an opportunity for functional recovery after stroke, if the most appropriate strategies are learnt and the maladaptive ones unlearnt [24].
There is now a growing understanding about how the body affects learning. The embodiment hypothesis proposes that sensorimotor activity of the person as it interacts with the environment is central to the development of intelligence [23]. In this field of study, the six principles of learning that babies instinctively follow can be summarized as under [23]:
Being multi-modal.
Being incremental.
Being physical.
Exploring.
Being social.
Learning a language (symbolic representation).
A multi-modal experience of the world is achieved in humans through the sensory system which is made up of a vast array of sensors to provide vision, audition, touch, smell, balance, and proprioception. Any single function can be accomplished by more than one signal configuration from the neurons and different neuron clusters need not be limited to a single function. This type of redundancy ensures continuity in function where parts of the network can learn from each other without an external teacher.
The second characteristic is the time-locked correlations between several simultaneous inputs, which are a powerful tool for representation, both singly and in combination with various events and objects in the environment [25]. In real-time these activities are mapped to each other to discover “higher order regularities,” for example, using a combination of touch and vision to understand texture or transparency.
In non-incremental learning, the entire training set is usually fixed and then presented in entirety or randomly sampled. However, it seems that systematic changes in the input patterns and their overlapping occurrence in time play a large part in determining the development process. As a child grows, the vision starts to couple with the hearing and helps organize attention. In hearing-impaired babies, we see disorganized attention and a consequent slower learning (this is common in stroke cases, where patients experience sensory overload and cognitive deficiencies). Co-ordination is a form of mapping of multi-modal learning and the way they map changes over the development time, using either changing patterns or additional sensory inputs which the infants are now able to voluntarily provide themselves through physical exploration. Shifts in inputs thus result from the infant’s own behavior. Using the body and moving from one place to another presents new spatial-temporal patterns and alters the infant’s perception of “objects, space and self.” Experimental studies show that one of the factors that strongly influence biological intelligence is “ordering the training experiences in the right way” [26].
Experiments by Ballard et al. [27] and Baldwin [28] show that children off-load short term memory to the world by linking objects and events to locations, using attention to selectively point to the world. It is an easy way to build coherence in the cognitive system and to keep contents of different information clusters separate from each other.
Initially the baby does not know what there is to learn. Babies can discover both the tasks to be learned and the solution to those tasks through exploration or non-goal directed action. One of the ways of exploration is spontaneous movement. As they contact objects in the environment, they progress from non-reaching to reaching. Thus, they seem to move from arousal to exploration to a selection of solutions from whatever space they can explore, which initially is limited. This type of learning is possible because of the multi-modal sensory system that builds maps from time-locked correlations starting with smaller spatial maps and expanding to larger ones.
In early interaction with mothers, infants learn from a pattern of activity that tightly couples vision, audition, and touch to behavior. Mother and infant imitate each other to reinforce this coupling. A mature social partner can also build a cognitive framework by weaving their own behavior around the child’s natural activity patterns. This is done by automatically selecting those patterns which they consider meaningful and helpful for the baby. They also serve to direct attention to an object or event to strengthen the coupling. This is done in the spatial as well as temporal aspects. The baby frequently looks for physical and directional support to manage the risks around exploration, to rest when tired and to crystallize goals through such imitation and coupling.
Language can be a regularity that is a “shared communicative system.” It is also a symbol system where the relation between the symbol and events in the world are mainly arbitrary, e.g., there is no relation between the word “dog” and what it represents, by knowing the word we cannot know the animal. DeLoache [29] demonstrated the way children use scale models and pictures as symbols which are not too life-like. Children first learn subtle regularities from the words they absorb, and slowly it creates in them the ability to learn a word in one trial and do higher-order generalization. Efficient learning through a form of language thus itself becomes learned behavior.
While new born babies have non-goal directed exploratory behavior, they soon graduate into a more goal-directed behavior. These goals are a result of their decision-making process which takes inputs from their emotions, knowledge, intelligence, and social partners (in this case maybe parents or elder siblings). The mature partner moderates the child’s emotions and value system and therefore, his or her early decisions during the learning process. This may be done through instruction, dialogue, feedback, and body language.
When this is considered in the context of a stroke patient, the goals he or she sets for recovery would be influenced by the same factors and more so with increasing disability and physical and emotional dependence. If we break down the learning process into its two broad components, exploratory and goal-directed, then one can line up the two components as an illustration shown in Figure 1. The patient formulates a goal (as in recovery of a specific function such as eating) and can begin exploratory learning in that specific context. However, there may exist cognitive as well as physical and social constraints due to post-stroke disability. If a technology could augment these aspects so that constraints are reduced through an appropriately designed user interface, it may facilitate such a patient re-booting how he learnt as a baby.
A composite learning behavior using the mind and physical body in a multi-modal fashion for goal-oriented exploration.
The goal dictates the quality, direction, and extent of the exploration. In stroke patients, the immediate and longer-term goals that the patient sets for himself/herself could significantly affect extent and speed of recovery [30]. Behavior generation is built around a distributed network of responses such as approach, play, avoidance of obstacles and attention requisition, all of which may be affected adversely after stroke. Behaviors may excite or inhibit each other, where non-conflicting behaviors fire motor commands with the brain and muscle complementing each other in real-time.
In a learning environment which requires multiple repetitions, not all of which are identical, as in re-learning a skill, Figure 1 forms the basic element of the learning iterations. Several iterations will be required as part of the exploratory strategy over time, which may be represented by a cyclic model as shown in Figure 2. In this figure, the feedback and feedforward loops drive subsequent iterations, which may be similar or dissimilar. Goals and decisions, as a feedforward, drive multi-modal exploration. Incremental changes or achievements seen at brain and body levels through measurable and quantifiable feedback drive modifications in belief systems, thus impacting goals and decisions for further learning.
The proposed natural learning model using iterative, incremental changes.
However, such faculties of learning available to a normal person may or may not be available to a stroke patient. A typical stroke model adapted from Ito et al. [31] of how stroke affects the human system resulting in motor function impairment is shown inFigure 3 with an augmentation of such impaired feedforward and feedback superimposed. In this figure, the pathways for motor commands from motor cortex and proprioceptive feedback from the musculoskeletal system are disrupted and hence, some alternate pathway is recommended shown by the “motor intention” and “motor actuation” blocks. This is a popular model implemented by the rehabilitation robotics community and those adopting the stimulation approach. Motor intention is usually sensed by a brain-computer interface or artificially induced by stimulation methods such as transcranial magnetic stimulation. Motor actuation is achieved by either electrical stimulation or mechanically driven robotic movement. Intention and actuation are bridged typically by some adaptive algorithm which may be based on feature extraction, a control strategy, and a feedback loop. Current technology, however, is not able to address the complex issue of hand function, which involves overlapping neuro-physio strategies and multiple degrees of freedom. At most, simple movements may be possible [32] which has been shown to not adequately impact function for the highly heterogeneous stroke affected population. Gross movements can be expected to improve with very high number of repetitions, thus enabling the brain to rewire itself in a limited way. However, there is poor evidence that such gross movement practice translates significantly into function. Therefore, the modification to the above model is proposed, incorporating the feedforward and feedback elements modeled in Figure 2 as a form of augmentation to help overcome the deficits through the learning route.
The self-regulated model of recovery of motor impairment after stroke adapted from Ito et al. [31].
The augmented feedback may be delivered visually via a muscle-brain-computer interface. The feedforward in the form of appropriate audio-visual inputs, which lead the human to attempt a series of desired actions through imitation, is known to facilitate recovery [33]. Moreover, there is evidence of perception transferring to action and more importantly, from action to perception [34]. The augmented feedback is expected to drive motor intention and exploration while the feedforward is expected to prime the brain for motor actuation and goal directed learning through imitation. From a functional improvement perspective, the augmented feedback may be customized for a person using time-locked parameters as follows:
EMG agonist-antagonist balance (muscle strategy).
EEG relaxation and attention states (brain strategy).
The brain and the body are inseparably linked, and both contribute significantly for neuroplasticity to occur and health parameters to improve [35]. Based on this understanding of how human learning may be applied practically in the context of post-stroke rehabilitation, this study was conceived with the following assumptions:
When EEG and EMG signals during activity are brought together in a time-synchronized manner for real-time feedback along with an audio-visual feedforward for imitation, it provides an opportunity for the patient to work with sensory, exploratory and goal-directed learning toward functional rehabilitation goals.
Displaying quantified, relative brain and muscle feedback in real-time while training activation and relaxation simultaneously during movement or while attempting to manipulate objects, will enhance the conditions for incremental associative learning of overlapping brain and muscle strategies to occur [36]. Under such conditions, subjects may potentially achieve systemic gains in functional performance, even though they may have tried existing rehabilitation methods and only partially succeeded.
This paper describes a bio-mechatronics approach to understanding where re-learning is misled or failing and uses a “feedforward-feedback” modality to help chronic stroke subjects train gross movements (as measured by Fugyl Meyer Upper Extremity Motor Assessment scale) and functional, timed-task capabilities (as measured by Action Research Arm Test). The SynPhNe system employs learning and training principles similar to that which babies seem to use in the design of its user interface, to leverage the mechanism of “self-regulation” or “self-correction.” The study explores to what extent such real-time “self-correction” alone, in the absence of any form of external stimulation or robotic assistance, impacts the recovery of functional ability in the stroke impaired, as a prelude to building a safe, effective, easy-to-use technology which would be useful for patients to augment therapy hours at home.
At the time of development, motor theory, learning principles and stroke rehabilitation challenges listed in Section 1 suggested that the SynPhNe rehabilitation platform should facilitate such learning keeping in mind the constraints faced by stroke patients.
EEG and EMG biofeedback with video-based feed-forward provided the multi-modal environment.
Incremental learning—use of biofeedback to highlight small changes in the muscle and the brain signals with their transitions and associating this with the gross movements and tasks performed with various degrees of success.
Exploratory learning, using the hand for real world tasks perceived as important but difficult (for example, use of chopsticks), as well as understanding how to achieve various relaxation and attention states while in dynamic movement using the feedforward-feedback modality.
Simulation of a “mature social partner” or instructor, perhaps in the form of an instructor led video which a patient could watch and follow and the smiley icon which indicates the successful management of the desired brain state while executing physical tasks.
Teaching a new, universal language, i.e., making the subject aware of how to interpret and self-regulate muscle and brain activity at a signal level.
Following the cyclic learning process shown in Figure 2, as a sensory-led, intuitive, self-sustaining, and reinforcing cycle.
The wearable data capture unit (WDCU) acquires data from eight channels of EMG through an arm gear and eight channels of EEG data through a head gear and transmits the data simultaneously to the PC using a USB cable (Figure 4). The design of this arm gear has been previously reported in a separate paper by the authors along with design and testing of the amplification circuit [37]. The software running on the PC processes these signals from 16 channels and combines them in a time locked manner for presentation on the screen as real-time feedback showing muscle over-activation and under-activation as cartoon characters (EMG signal as agonist-antagonist koala bears climbing up or down a tree, EEG signal as a smiley face). While EMG signals are used as feedback by squaring and averaging the amplitude within a running window updated every 10 milliseconds, the EEG signals were converted to frequency band using a Fast Fourier Transform and the alpha band power (8–13 Hz) was used to represent a relaxed state, updated every 10 s as a proportion to total power in the 1–35 Hz frequency band. While EMG was sampled at 1000 samples/sec, EEG was sampled at 256 samples/s.
SynPhNe learning model platform and user-interface.
The goal of both the feedforward and feedback is to successfully attempt a movement or physical task while maintaining a relaxed brain-muscle state pre- and post-action comparable to resting state. If effort results in a deviation from resting state, return to resting state post-effort should be immediate. Brain and muscle influence each other too. Losing attention partially or fully may result in loss of ability to imitate the feedforward video and respond to feedback. Incremental changes in self-regulation are presented visually in the real-time user interface, which then provides an impetus for the patient to self-regulate further.
Figure 4 depicts the user interface on the computer screen. The subject observes the video as the feedforward in order to imitate it with the same speed. The koala bears, and tree serve as agonist and antagonist muscle EMG feedback during such imitation. The subject attempts to activate the appropriate muscle to raise the brown bear (agonist) to the top of the tree while keeping the gray bear (antagonist) as steady and close to the bottom of the tree as possible. The yellow smiley face represents EEG frequency band feedback as a measure of a relaxed brain state which needs to be maintained as best as possible while imitating the video-based physical movement or task.
In both the clinical studies, the subject tried to imitate an exercise and task practice video sequence running on the computer screen, while attempting to correct maladaptive over-activation and under-activation in opposing muscle pairs displayed on the same screen. Using a slower speed of execution than normal allowed proximal joints of the upper limb to stabilize and reduce temporal demands on the subject [38]. The slow-paced video sequences allowed time to train relaxation between repetitions. Also, the need to achieve a relaxation goal immediately after activation encouraged the subjects not to over-activate the muscles and to moderate their effort. This strategy was found to delay the onset of high dynamic muscle tone and allow for better repetition-based performance based on greater number of successful relaxations. When subjects experienced difficulties in being able to relax their muscles, they intuitively made postural corrections to let go and relax deeper before the next muscle activation. EMG thresholds displayed on the software gave them a clear indication on activation and relaxation targets appropriate for training, which were based on previously calibrated maximum voluntary contraction (targets were up to 40% of maximum) and resting state EMG respectively, for various muscle groups. In this paper, analysis of only the EMG peaks data as seen during activity and immediately post activity repetition is highlighted. The EEG and other metrics will be reported separately in subsequent papers since the primary objective of this paper is to highlight the thinking behind the user-interface design and the pre and post clinical outcomes.
In Trial 1, 15 adult chronic stroke subjects with a hemiplegic hand (31–69 years; 4 females, 11 males) were recruited for the study (Table 1). In Trial 2, 10 adult chronic stroke subjects with a hemiplegic hand (45–69 years; 1 female, 9 males) were recruited for the study (Table 1).
Subject code | Age | Gender | Months poststroke | Nature of stroke |
---|---|---|---|---|
Demographics of subjects in Trial 1 | ||||
RH001 | 57 | Female | 22 | Hemorrhage |
RH002 | 44 | Male | 21 | Infarct |
RH003 | 54 | Male | 12 | Infarct |
RH004 | 61 | Male | 25 | Infarct |
RH005 | 69 | Male | 21 | Infarct |
RH006 | 38 | Male | 18 | Hemorrhage |
RH007 | 48 | Male | 18 | Hemorrhage |
LH001 | 31 | Female | 32 | Infarct |
LH002 | 53 | Female | 18 | Hemorrhage |
LH003 | 59 | Female | 37 | Infarct |
LH004 | 62 | Male | 8 | Infarct |
LH005 | 57 | Male | 10 | Hemorrhage |
LH007 | 65 | Male | 45 | Hemorrhage |
LH008 | 62 | Male | 15 | Hemorrhage |
Mean | 54.3 | 21.6 | ||
Std. dev. | 10.3 | 10.0 | ||
Demographic details of subjects in Trial 2 | ||||
NRH001 | 69 | Male | 21 | Infarct |
NRH002 | 60 | Male | 28 | Infarct |
NRH003 | 57 | Female | 23 | Hemorrhage |
NRH004 | 59 | Male | 7 | Infarct |
NRH005 | 65 | Male | 7 | Infarct |
NRH006 | 46 | Male | 60 | Hemorrhage |
NRH007 | 67 | Male | 49 | Infarct |
NLH001 | 61 | Male | 21 | Infarct |
NLH002 | 45 | Male | 49 | Infarct |
NLH003 | 62 | Male | 69 | Infarct |
Mean | 60.0 | 32.3 | ||
Std. dev | 7.6 | 20.7 |
Demographic of recruited subjects.
Both left and right limb impaired subjects were included for a better patient representation with at least 6 months post a first clinical stroke. Only paralysis with M.R.C. grade between 1 and 3 at elbow and digits was considered for inclusion. Passive, pain-free range of motion was at least 50% in all below elbow joints. No exclusion was made based on type of stroke and the group included those with ataxia and tactile sensory loss.
The experiments had only treatment group whose members had plateaued (those who had completed the rehabilitation program recommended by the hospital) in functional recovery and were ready to discontinue any other form of regular or alternative therapy during the study.
In Trial 1, the subjects were randomized between two clinical therapists, where either of them could conduct any session for any subject (as is common in a typical clinical setting). In Trial 2, to simulate a home-based, non-clinical environment, the therapy was not conducted in a standard hospital therapy/rehabilitation ward but rather in a normal spare room with a table and a chair. A research associate with a non-therapy background was trained to operate the SynPhNe system to deliver the sessions every day.
Each subject completed a 4-week, 3 sessions/week protocol using the automated SynPhNe device which delivers the learning modality. Each session lasted for 50–75 min including the setup time. In Trial 1, the EEG signals were captured during three sessions to track changes, i.e., in the beginning, midway and end of the study whereas in Trial 2, the EEG signals were captured in all 12 sessions, with the smiley face retained as a form of feedback on relaxed brain state represented by the relative alpha-band power as calibrated at rest. This brain-based feedback was introduced after it was observed that a significant component of therapist supervision in Trial 1 consisted of repeatedly nudging the subjects’ attention back to task.
Imitating the video, subjects performed four basic hand movements—wrist extension and flexion, finger extension and flexion, pronation and supination, and open grasp. This was followed by four everyday tasks—picking up a pen, flipping a page, grasping a bottle and use of chopsticks (Figure 5).
Task practice (1) picking up a pen, (2) grasping a bottle, (3) flipping a page, (4) using a pair of chopsticks (pictures extracted from the instructional video created for the experiment).
These four tasks were chosen to represent a two-finger pinch with pronation, a cylindrical grasp, a key pinch with pronation and supination and a five-finger pinch which demands attention. Each exercise was repeated five times in the first three sessions and 10 times in the subsequent sessions while attempting to maintain a pre-calibrated agonist-antagonist balance using the biofeedback. In Trial 1, some of the more severely affected subjects (n = 7) were provided the facility for an automated triggering of electrical stimulation on extensor muscles for some or all sessions if the subject achieved an agonist EMG threshold while maintaining a relaxed antagonist [39]. In Trial 2, we did not use any FES as Trial 1 indicated that FES induced exaggerated, instantaneous antagonist-side reactions, which our protocol was, in fact, trying to minimize.
Pre-, mid-, and post-outcomes were measured using standard clinical scales [Fugl Meyer Upper Extremity Motor assessment (FMA) and Action Research Arm Test (ARAT)] to assess both gross and fine movements [40]. They were also randomized for assessment between two other therapists who were blinded to the study protocol. All subjects provided a signed written consent. Ethics approval was obtained from the Institutional Review Board of National Healthcare Group, Singapore. The set-up for the two experiments is shown in Figure 6.
Clinical trial setup in (A) Trial 1 (therapy ward) and (B) Trial 2 (outside therapy ward).
On comparing the muscle activation and relaxation scores across all subjects in Trial 1 (168 sessions) and Trial 2 (total 120 sessions), it was seen that successful performance of higher repetitions of muscle contractions above an EMG threshold was associated with the ability to volitionally relax those muscles below an EMG threshold immediately after contraction (Trial 1: Pearson’s coefficient = 0.78, CI = 99%; Trial 2: Pearson’s coefficient = 0.74, CI = 99%).
Subjects who were unable to relax, volitionally, in a consistent manner had difficulties in performing simple actions such as extensions and flexions repeatedly as well as tasks. The antagonist was observed to be relatively stronger (the gray koala bear climbed higher up on the tree) in most subjects at week 0, whenever the subjects tried to activate the agonist and raise the golden koala bear up the tree. These subjects also demonstrated an inability to relax a muscle immediately on completion of a movement or task.
The outcomes based on the FMA and ARAT clinical scales for both the trials are summarized in Table 2. Subjects have been categorized into mildly- (55–57), moderately- (32–54) and severely-impaired (≤31) based on their FMA scores at week 0. Subject LH006 encountered a personal accident at home resulting in a head injury during the study and was discontinued from the trial.
Impairment level | Subject code | Fugl Meyer (FMA) | Action research arm test (ARAT) | ||
---|---|---|---|---|---|
W0 | W4 | W0 | W4 | ||
Clinical outcomes in Trial 1 | |||||
Mild | RH001 | 58 | 60 | 53 | 57 |
Moderate | RH003 | 36 | 44 | 9 | 11 |
RH005 | 45 | 46 | 20 | 27 | |
RH007 | 50 | 59 | 45 | 49 | |
LH001 | 35 | 33 | 5 | 5 | |
LH002 | 44 | 45 | 25 | 28 | |
LH004 | 45 | 44 | 21 | 21 | |
LH005 | 52 | 56 | 32 | 39 | |
LH007 | 50 | 52 | 32 | 44 | |
LH008 | 43 | 47 | 32 | 32 | |
Severe | RH002 | 16 | 19 | 6 | 7 |
RH004 | 27 | 27 | 5 | 5 | |
RH006 | 29 | 31 | 17 | 17 | |
LH003 | 22 | 24 | 3 | 9 | |
Mean | 39.43 | 41.93 | 21.79 | 25.07 | |
Std. dev | 11.86 | 12.67 | 15.10 | 16.64 | |
Clinical outcomes in Trial 2 | |||||
Moderate | NRH006 | 54 | 56 | 38 | 51 |
NLH003 | 43 | 42 | 17 | 23 | |
NLH002 | 38 | 41 | 25 | 28 | |
NRH001 | 38 | 40 | 18 | 25 | |
NRH007 | 37 | 39 | 21 | 26 | |
NRH004 | 37 | 39 | 27 | 31 | |
NRH003 | 32 | 33 | 7 | 13 | |
Severe | NRH005 | 31 | 30 | 9 | 10 |
NRH002 | 20 | 24 | 8 | 9 | |
NLH001 | 19 | 20 | 3 | 4 | |
Mean | 34.90 | 36.40 | 17.30 | 22.00 | |
Std. dev | 9.78 | 9.69 | 10.31 | 13.05 |
FMA and ARAT clinical scores at week 0 (W0) and week 4 (W4).
The scores for both the assessment scales were reduced to a common denominator by normalizing assessment scores against full scores of the respective scale. For FMA and ARAT, the full scores are 66 and 57 respectively.
Based on the nominalized scores, the percentage improvement in both the functional scales for the subjects in Trial 1 and Trial 2 can be summarized as shown in Table 3. Since these improvements are based on initial measurements of level of impairment (week 0), they capture both clinical and sub-clinical performance changes or incremental improvements or decline achieved by the subjects. The estimated minimum clinically important difference (MCID) of the upper limb FMA scores ranges from 4.25 to 7.25 points depending on the different facets of upper limb movement (overall upper limb function MCID is 5.25) while the MCID values for the ARAT were 5.7 points for chronic stroke patients [41, 42]. In Trial 1, there were two subjects who achieved MCIDs in FMA; RH003 (8 points) and RH007 (9 points) and four subjects who achieved MCIDs in ARAT; RH005 (7 points), LH005 (7 points), LH007 (12 points), LH003 (6 points). In Trial 2, subjects NRH006 (13 points), NLH003 (6 points), NRH001 (7 points) and NRH003 (6 points) achieved MCIDs in ARAT. These MCIDs were achieved with only 5–10 repetitions per exercise per session, which is about 10–30% of the number of exercise repetitions recommended per session in standard care.
Subject code | Fugl Meyer (FMA) | Action research arm test (ARAT) |
---|---|---|
Percentage improvement in Trial 1 | ||
RH001 | 3.45 | 7.55 |
RH002 | 18.75 | 16.67 |
RH003 | 22.22 | 22.22 |
RH004 | 0.00 | 0.00 |
RH005 | 2.22 | 35.00 |
RH006 | 6.90 | 0.00 |
RH007 | 18.00 | 8.89 |
LH001 | −5.71 | 0.00 |
LH002 | 2.27 | 12.00 |
LH003 | 9.09 | 200.00 |
LH004 | −2.22 | 0.00 |
LH005 | 7.69 | 21.88 |
LH007 | 4.00 | 37.50 |
LH008 | 9.30 | 0.00 |
Mean | 6.85 | 25.84 |
Std. dev | 7.85 | 49.87 |
Percentage improvement in Trial 2 | ||
NRH001 | 5.26 | 38.89 |
NRH002 | 20 | 12.5 |
NRH003 | 3.13 | 85.71 |
NRH004 | 5.41 | 14.81 |
NRH005 | −3.23 | 11.11 |
NRH006 | 3.7 | 34.21 |
NRH007 | 5.41 | 23.81 |
NLH001 | 5.26 | 33.33 |
NLH002 | 7.89 | 12 |
NLH003 | −2.33 | 35.29 |
Mean | 5.05 | 30.17 |
Std. dev | 5.72 | 20.22 |
Percentage improvement post-therapy (week 4) with respect to pre-therapy.
Training in self-regulation of antagonist muscle relaxation during movement using the SynPhNe system contributed to positive pre-post changes in FMA (Trial 1: Mean = 6.855%, SD = 7.85; Trial 2: Mean = 5.05%, SD = 6.00) and ARAT (Trial 1: Mean = 25.84%, SD = 49.86; Trial 2: Mean = 30.17%, SD = 21.20).
Results from the two separate trials are presented to illustrate the degree of consistency in two different patient samples. The inclusion and exclusion criteria in both studies were similar. However, in Trial 1 therapists fully supervised the therapy sessions while in Trial 2 non-therapists conducted the sessions. In both studies, a separate team of blinded therapists performed the pre- and post-assessments. Neither study reported any adverse events.
Figure 7 supported the research group’s direction that both activation and relaxation must be trained specifically, as opposed to a pre-occupation with repeated muscle activation alone as is common in rehabilitation [43].
Muscle activation is associated with relaxation during repetitive practice in (A) Trial 1 (B) Trial 2.
Both the studies reported a larger increase in ARAT scores as compared to FMA scores. This increase in ARAT was not necessarily linked to those who had high FMA scores at week 0. This suggests that functional task performance and object manipulation ability may improve even though reduction of impairment at a gross level is proportionately lower. Subjects who achieved MCIDs did so mostly in ARAT and not FMA, which is somewhat counter-intuitive. This may be because several functional tasks do not demand a full range of motion, e.g., Eating with chopsticks or Picking up a small object like a pen with a two-finger pinch. In the experience of the study team, it was noted that subjects were more motivated attempting to do actual functional tasks such as opening a book and manipulating chopsticks as compared to standard joint extension/flexion exercises that were repetitive and not directly linked to a perceived functional outcome. It may be noted that each exercise and activity was repeated only 5–10 times per session to produce the outcomes reported, which was about a fifth of the number usually recommended in rehabilitation settings, and about a tenth or less of that in high repetition therapy. This was done to ensure that compensatory strategies did not set in due to fatigue, boredom, or distraction. The results raise some questions about initial functional results being dependent on high repetitions and are, in fact, reminiscent about how babies learn with few, non-similar repetitions [29]. Since both studies exclusively recruited patients who were both chronic and plateaued, the chances of spontaneous recovery were minimized, although cannot be ruled out. The authors are of the opinion that restoration of function resembling spontaneous recovery may, in fact, be facilitated in the chronic phase of therapy by the re-learning of such brain and muscle strategies as described in these experiments, enhancement of relaxation and attention and the progressive reduction of compensation.
The gold standard for restoration of function and independence is still conventional, manual therapy. Kollen et al. reviewed more than 700 published studies and concluded that conventional robotic or stimulation treatment approaches induce improvements that are confined to impairment level only and do not generalize to functional improvement [2]. They stated that treatment strategies that incorporate a strong emphasis on functional training and task-specific therapy may hold the key to optimal stroke therapy. A search of systematic reviews in the Cochrane and other databases on well-known approaches such as electro-mechanical and robot-assisted arm training, electro-stimulation and EMG triggered neuromuscular stimulation of wrist and fingers showed that only electro-stimulation held certain advantages over conventional, manual therapy when comparing outcomes for motor ability [44, 45, 46, 47, 48]. However, conventional therapy continues to be superior in improving the complete spectrum ranging from gross motor, fine motor, strength, dexterity and ability to manipulate objects and perform timed tasks. Hence, the authors of this paper carried out a follow-up study with 30 subjects, comparing a group undergoing SynPhNe training to a group receiving standard care, which was a mix of conventional physiotherapy, physical therapy, occupational therapy and neuro therapy. Since the goal is to develop a system which can augment therapy effectively at home, the study was designed to prove that SynPhNe treatment was comparable to standard care. The results of this study have been published previously [49]. The conclusion was that SynPhNe training was comparable to standard care as seen in the FMA and ARAT scales.
The EMG data demonstrated that the stroke subjects had hitherto unknown antagonist over-activation in wrist and finger movements, which were moderated and subdued by starting the exercises with a reduced range of motion and reduced speed. Once the antagonist activity was subdued and reinforced over 2–4 sessions, the range of motion and speed was progressively increased in subsequent sessions. This was effective particularly in wrist and finger extension, which is known to be a significant challenge for most stroke patients. Control deficiencies in approach, sequential steps and object release were similarly improved with slower execution speeds that were meant to effect better proximal stabilization and reduced compensation as often seen in shoulder elevation and abduction while reaching, pronating, and grasping with the affected arm. Since the most significant improvements in percentage terms were seen in the ARAT scale which evaluates functional and participation tasks, the authors propose that the SynPhNe system impacts independence positively, combined with enhanced self-regulation and the self-use of technology.
All subjects tolerated the multi-modal feedback well and did not report feeling overwhelmed by the user interface and demands of the feedforward-feedback loop. It was noticed that the distribution of the visual sampling of the feedforward and feedback during the sessions differed between subjects and within subjects as therapy sessions progressed. This could be an interesting area of investigation in future studies to better understand how adults learn in a non-instructional and sensory manner. This paradigm needs to be tested further with a larger study and a 30–60 day follow-up to evaluate retention of brain-muscle strategies learnt and further generalizations to other functional activities. Two larger, case-controlled studies are underway presently with sub-acute and chronic phase patients to understand how the transition from hospital to home-based therapy may be executed using the SynPhNe system, and the effect on outcomes and independence.
Training to relax specific muscles adequately and in a timely manner during therapy using a feedforward-feedback loop, instead of practicing repetitive muscle contraction alone, may help re-learn movement and daily functional activities in stroke subjects who have “plateaued” and not responding to further therapy.
Simultaneous activation-relaxation training of agonist-antagonist not only facilitated improvement of functional abilities but was also well tolerated by all subjects and did not cause them to get overwhelmed by the number of feedforward and feedback elements on the computer screen. This indicated that despite the challenges brought on by stroke, patients with impairments can still leverage their sensory learning abilities in an exploratory and then goal-directed manner while attempting to regain spatial and temporal aspects of movement and function of the upper limb. Thus, they appeared to be able to re-boot how they learnt in a sensory manner as babies using the feedforward-feedback modality. A wearable device such as the SynPhNe system may, therefore, help leverage neuroplasticity and act as a key complement to conventional therapy. Being patient-led and requiring reduced therapist supervision, it can effectively augment therapy hours at home or in the community, thus holding the promise of making daily therapy accessible and affordable to all.
The research was funded by the National Research Foundation POC Grant and Singapore-MIT Alliance for Research and Technology (SMART) Innovation Grant, both in Singapore. Our thanks also go out to the subjects who participated and the clinical teams at Tan Tock Seng Hospital and National University Hospital, Singapore.
Subhasis Banerji and John Heng are founders and inventors of the SynPhNe system. While providing technical support and supervision to the studies, they were blinded to pre- and post-clinical assessment of subjects.
Daphne Menezes and Ponvignesh Ponnusamy are current employees of Synphne Pte. Ltd., Singapore. Daphne Menezes assisted the clinical study team as a trainer in the SynPhNe system and observer of therapy sessions. Ponvignesh Ponnusamy assisted with software programming and user interface development only. Both were blinded to pre- and post-clinical assessment of subjects.
The other authors have no conflict of interest.
Heterosis is the superiority of F1 offspring over either parent, a solitary means of harnessing complete hybrid vigor in crop plants. This phenomenon has aided agriculture and captivated geneticists for over centuries for the development of superior cultivar in many crops [1]. Suitable allelic combination and manipulation has made yield advantage in hybrid than HYVs. It covers large acreage for many crops, including rice, and has affected agrarian practices and the seed business across the world. Heterosis had been exploited in several practical ways for centuries before Darwin provided an early scientific explanation in maize. In rice, heterosis was first reported by Jonse [2]. However, owing to its self-pollinating nature (0.3–3.0% out-crossing), heterosis could be realized during middle of second half of the twentieth century after identification and development of the cytoplasmic male sterile (CMS) source. Subsequently, China, under the leadership of Yuan Long Ping, started work on the development of hybrid rice (HR) with a vision to make it possible to be commercial. He identified a natural male sterile mutant plant in rice (indica) and pollen abortive genotypes in the wild rice (Oryza rufipogon; Li 1970), which later served as donor of male sterile source (male sterile cytoplasm) for CMS development. In 1973, through recurrent back-cross breeding, several promising indica wild abortive CMS, viz., Erjiunan1A, Zhenshan 97A, and V20A CMS-WA, and good restorers, viz., Taiyin1, IR4, and IR1, were developed. Later during 1974, first indica rice hybrid, Nanyou 2, was released for cultivation in China. Afterward, relatively more heterotic hybrid rice (HR) breeding approaches like two-line system (1987 AD) and super hybrids (1996 AD) were adopted which supplemented substantially toward Chinese food security and livelihood.
\nIn India, systematic research on hybrid rice was initiated during 1989 when the Indian Council of Agricultural Research (ICAR) launched a special goal-oriented and time-bound project, “Promotion of Research and Development Efforts on Hybrids in Selected Crops,” for rice at 12 network centers. Around 4 years (1989–1993) of rigorous research efforts have rewarded substantially, and India became the second country after China to develop and commercialize hybrid rice. The first hybrid variety APRH-1 was released by APRRI, Maruteru, for Andhra Pradesh in 1993–1994. So far, 117 rice hybrids (36 from public organization and 81 from private sector) were developed, suitable for different ecology and duration ranging from 115 to 150 days, covering 3.0 mha, which accounted for ~7.0% of the total rice acreage in India (Varietal Improvement, Progress report) [3].
\nHybrid rice technology has substantial yielding ability that is able to enhance farm productivity ~15–25% more than inbred varieties. Given its yield advantage and economic importance, several hybrids in rice have been commercialized in more than 40 countries, which has created a huge seed industry worldwide. Moreover, this venture also has great service opportunity and generates additional employment for the poorer [1]. However, it has some limitations in generation of hybrids, seed production, and marginal heterosis. Success of the hybrid depends on their parental combination, adaptability, and allelic interactions, and hence, faces several problems like unstable male sterility (MS), non-abundancy in cytoplasmic diversity, inherited CMS load, low seed producibility in seed parent, poor grain and eating quality, lack of responsive parents for biotic and abiotic stresses, hybrid sterility, marginal heterosis in indica hybrids, etc. This chapter deals with information on: (i) research status of HR, (ii) breeding system and methods involved in hybrid rice development and production, (iii) trait-specific parental line improvement, (iv) molecular dissection of genes and QTLs for parental line improvement, and (v) economic opportunity (Figure 1).
\nA schematic representation of hybrid rice technology (seed production, trait improvement, yield evaluation, etc.).
Rice is a strict self-pollinated crop; commercial exploitation of heterosis requires some parental specificity which could excludes manual emasculation. The invention of naturally occurred male sterility (MS) in rice thus played substantial role in realization of heterosis in rice. Following are the genetic tools as mentioned in various heads are required for development and commercialization of hybrid in rice:
\nThe male sterility (MS) in plants is the condition where the male reproductive organ, anthers, loses its ability to dehisce and produce viable pollen and thus encourages the allogamous nature of reproduction. This is crucial breeding tools to harness heterosis that exclude additional efforts of emasculation which is cumbersome process. In plants, male sterility is conditioned either by mitochondrial or nucleus genome or in associations. The male sterility in plant was first observed by Joseph Gottlieb Kolreuter in 1763 and later it was reported in >610 plant species. In rice, it was reported by Sampath and Mohanty [4] at ICAR-NRRI (formerly CRRI), Cuttack by studying the differences in male fertility in indica/japonica reciprocal crosses. The male sterility in plant is found to be determined by several biological as well as environmental factors. In rice, it is conditioned either by cytoplasmic genes in association with nuclear genes (CMS) or nuclear genes alone (GMS) which cause abnormal development in sporogenous tissue (either sporophytic or gametophytic tissue). The sporophytic male sterility is governed by genetic constitutions of sporogenous tissues like tapetal and meiocytes which creates improper nourishing to developing microspores and cause pollen abortion, whereas in gametophytic male sterility, microspore and pollen development get affected. Sporophytic male sterility is quite useful in hybrid rice breeding as it gets fertile in heterozygous state and encourages complete fertility in resulting hybrids. To date, several types of male sterile system, viz., cytoplasmic male sterile (CMS), environment sensitive male sterile (GMS), viz., thermo-sensitive genetic male sterility (TGMS), photo-sensitive genetic male sterility (PGMS) and reverse photo-sensitive genetic male sterility (rPGMS), etc. have been identified and substantially being utilized in hybrid development (Table 1).
\nCMS group | \nAssociated ORF | \nProtein | \nCytoplasm source | \nRepresentative CMS-line | \n
---|---|---|---|---|
\n
| \n||||
\n
| \n||||
BT-CMS (G) | \n\nB-atp6-orf79\n | \nMembrane protein | \nChinsurah Boro II/Taichong 65 | \nLiming A, Xu 9201A | \n
LD-CMS (G) | \nUK | \nUK | \nLead Rice (Burmese indica variety) × Fujisaka 5 (japonica variety) | \nFujisaka 5A | \n
Dian1-CMS (G) | \nUK | \nUK | \nYunnan high altitude landrace rice (indica) cytoplasm | \nYongjing2A, Ning67A | \n
HL-CMS (G) | \n\natp6-orfH79\n | \nMembrane protein | \nRed-awned wild rice (Oryza rufipogon) cytoplasm | \nYuetai A, Luohong 3A4 | \n
\n
| \n||||
WA-CMS (S) | \n\nrpl5-WA352\n | \nMembrane protein | \nWild abortive rice (Oryza rufipogon) cytoplasm | \nZhenshan97 A, V20A, IR58025A, CRMS31A, etc. | \n
Kalinga-I-CMS (S) | \nUK | \nUK | \nKalinga-I (indica) cytoplasm | \nCRMS 32A | \n
D-CMS (S) | \nUK | \nUK | \n\nIndica rice Dissi D52/37 | \nD-Shan A, D62A | \n
DA-CMS (S) | \nUK | \nUK | \nDwarf abortive rice (Oryza rufipogon) cytoplasm | \nXieqingzao A | \n
GA-CMS (S) | \nUK | \nUK | \nGambiaca (indica) cytoplasm | \nGang 46A | \n
ID-CMS (S) | \nUK | \nUK | \nIndonesia paddy rice (indica) cytoplasm | \nII 32A, You1A | \n
K-CMS (S) | \nUK | \nUK | \nK52(japonica) cytoplasm | \nK-17A | \n
CMS-RT102 (S) | \n\nrpl5-orf352\n | \nMembrane protein | \n\nOryza rufipogon, W1125 | \nRT102A | \n
CMS-RT98A (G) | \n\norf113-atp4-cox3\n | \nMembrane protein | \n\nOryza rufipogon Griff, W1109 | \nRT98A | \n
LX-CMS | \nUK | \nUK | \nLuihui rice (indica) cytoplasm | \nYue 4A | \n
Maxie-CMS | \nUK | \nUK | \nMS mutant of Maweizhan (indica) with Xieqingzao (indica) | \nMaxie A | \n
NX-CMS | \nUK | \nUK | \nSelected from F2 male sterile plants in the progeny of Wanhui 88 (indica) × Neihui 92–4 (indica) nucleus | \nNeixiang 2A, Neixiang5A | \n
Y-CMS | \nUK | \nUK | \nYegong (indica landrace) cytoplasm | \nY Huanong A | \n
CW-CMS (G) | \n\norf307\n | \nMitochondrial protein | \n\nOryza rufipogon Griff. | \nIR24A, IR64A | \n
\n
| \n||||
PGMS | \n\npms3\n | \nNoncoding RNA | \nNongken 58S, PGMS mutant of japonica cultivar Nongken 58 | \n7001S, N5088S | \n
P/TGMS | \n\np/tms12–1\n | \nnoncoding RNA | \nPhotoperiod and temperature sensitive genic male sterile (P/TGMS) derived from Nongken 58S | \nPei’ai 64S | \n
TGMS | \n\ntms5, RNase ZS1\n(loss in function) | \nNuclease enzyme | \nSpontaneous TGMS mutants of Annong S-1 and Zhu 1S | \nGuangzhan 63S5, Xinan S | \n
rPGMS | \n\ncsa OsMST8 | \nMYB transcript regulator | \nCarbon starved anther (csa) mutant of japonica cultivar 9522 | \n9522S | \n
Cytoplasmic diversity in rice CMS.
Note: “S” stands for sporophytic male sterility and “G” stands for gametophytic male sterility.
The CMS is a maternally hereditary trait instigated by improper communication between cytoplasmic and nuclear genome [5]. Gene(s)/genic block(s)-conditioned cytoplasmic male sterility is chimeric construct, which evolved due to rearrangement of the mitochondrial genome (Figure 2). In rice, several types of CMS have been identified and characterized, having diversified mechanism in MS expression. Wild abortive (WA-CMS), a sporophytic MS system, is widely utilized in hybrid development. It is found to be caused by a constitutive mitochondrial gene WA352c located downstream of rpl5 (comprised four mitochondrial genomic segments, orf284, orf224, orf288, and cs4-cs6) and encodes a putative protein (352-residue) with three transmembrane segments. The WA352c inhibits nuclear-encoded mitochondrial protein COX11 (essential for the assembly of cytochrome c oxidase, TCA) and triggered premature tapetal programed cell death and pollen abortion [6]. In contrast, BT-CMS is a gametophytic MS reported in the Indian rice variety, Chinsurah Boro-II, in which pollen development get arrested at the tri-nucleate stage. The mitochondrial chimeric (dicistronic) gene B-atp6-orf79 encodes a transmembrane protein, cytotoxic peptideORF79 [7], which accumulates preferentially in the microspore, was found to be responsible for male sterility. The orf79 reside downstream to the atp6 and interact with P61 and mitochondrial complex III and impair the activity of this complex which lead to dysfunctional energy metabolism and elevate oxidative stress and thus causing sterility. However, in HL-CMS, which is also a gametophytic MS system, pollen development gets arrested at di-nucleate stage. A chimeric aberrant transcript of the mitochondrial geneatp6-orfH79, located downstream of atp6is confirmed as candidate gene of this MS. Transcript of orfH79 gene preferentially accumulates in mitochondria which interacts with P61 (a subunit of ETC complex III) and impairs mitochondrial function [8] and leads to MS. The MS in CW-CMS is conditioned by mitochondrial orf307, which causes anther-specific mitochondrial retrograde regulation for nuclear gene expression. It is a gametophytic MS in which pollen grain appears normal but unable to germinate.
\nSchematic presentation of rice CMS types, where WA stands for wild abortive, BT is for boro type, HL for Honglian, LD for lead rice, CW is for Chinese wild rice, RT102A and RT98A, respectively.
The GMS in rice is conditioned generally by recessive nuclear genes and exert showing normal Mendelian inheritance. Owing to difficulties in their maintenance (occurrence of only 50% sterility in F1), GMS could not be part of rice hybrid breeding program. Some GMS lines has shown threshold nature in MS expression where male sterility occurs in specific environmental regime (high temperature and long day length); hence called environment sensitive genetic male sterile (EGMS). The GMS line shows male sterility at elevated temperature, that is, >30°C is called temperature sensitive male sterility (TGMS) whereas male sterility in long day length, that is, >13.5 h is called photoperiod-sensitive genetic male sterility (PGMS). The male sterility in EGMS line is found to be revert into male fertile in favorable temperature (<30°C) and day length (<12.5 h) which provide its unique opportunity to be utilized in hybrid rice breeding program. The rice lines exert MS impression under long photoperiod and elevated temperature are referred as P/TGMS, for example, Pei’ai 64S. The EGMS lines, PGMS-Nongken 58S (NK58S) and TGMS-Annong S-1 and Zhu1S or derivatives are utilized extensively in majority (>95%) of the two-line hybrid program. Among, derivatives of NK58S are exerts either P/TGMS or even TGMS (e.g., Guangzhan 63S), the mechanism underlying to such dramatic changes yet to be revealed. Recently, a novel type of EGMS (csa-carban starved anther mutant) in rice called rPGMS (reverse PGMS). These lines expresses MS under short photoperiod (<12.5 h) and revert to normal fertile when exposed to long days (>13.5 h). This is found to be suitable for seed production of two-line hybrids in tropics and subtropics [9].
\nThe genetically engineered male sterile line M2BSin rice is developed by transformation of indica rice maintainer M2B with partial-lengthHcPDIL5-2a (Hibiscus cannabinus protein disulfide isomerase-like) genetic construct. Male fertility in this CMS is reported to be arrested due to tapetum degeneration which leads pollen abortion. The genetic analysis revealed this MS a maternally inherited inability as of CMS. Besides, by combining cysteine-protease gene (BnCysP1) of Brassica napus with rice anther-specific P12 promoter (promoter region of Os12bglu38 gene), a transgenic MS system was successfully created which is restored by transgenic rice plants carrying BnCysP1Si silencing system [10]. Zhou and co-workers [11] could develop 11 “transgene clean” TGMS lines by editing most widely utilized TGMS gene tms5 through CRISPR/Cas9.
\nThe rice CMS is found to be restored by nuclear genome, that is, mono or oligo nuclear loci called restorer gene. In rice, a total of 10 Rf genes (Rf1a, Rf1b, Rf2, Rf3, Rf4, Rf5, Rf6 and Rf17, Rf98 and Rf102) have been identified, of those seven (Rf1a, Rf1b, Rf2, Rf4, Rf5, Rf17, and Rf98) are characterized. All Rf genes are found to be dominant in nature (except Rf17, restores fertility in CW-CMS), which can restore male fertility in heterozygous state. Restorer genes are very specific to male sterile genome in the mechanism of fertility restoration. Genes Rf1a and Rf1b (Chr.-10) encode pentatricopeptide-repeat (PPR)-containing proteins and have functional affinity of fertility restoration in BT-CMS; RF1A promotes endonucleolytic cleavage of the atp6-orf79 mRNA andRF1B promotes degradation of atp6-orf79 mRNA [7] and revert the male sterility into fertility. Whereas, HL-CMS is restored either by Rf5 or Rf6 gene, these genes can produce 50% normal pollen grains in F1 plants individually; however, both genes in complementation could restore more than 80% spikelets’ fertility in hybrids. The Rf5 encodes a PPR family protein PPR791 and which bind with GRP162 (glycine rich protein) and atp6-orfH79 transcripts and makes a RFC (restoration of fertility complex). The RFC cleave the aberrant transcript of atp6-orfH79at 1169 nucleotides position [12]. TheRf6 gene encodes a novel PPR family protein (duplicate PPR motif 3–5) which in association with hexokinase (osHXK6) targets mitochondria and process defective transcript of atp6-orfH79 at 1238 nucleotide position. Thus, PPR protein family cause editing of aberrant transcript, inhibit their translation, and at the end, fertility restoration. Besides, male fertility in WA-CMS is found to be counteracted by Rf3 and Rf4 genes (chrom.-1 and 10, respectively). The genes Rf3 and Rf4 encode a pentatricopeptide protein (PPR) where RF4 cleave the abnormal WA352 transcript and RF3 suppress translation of WA352 into polypeptide and helps in restoring fertility in WA-CMS. Fertility in LD-CMS is reported to be restored by either Rf1 or Rf2. The Rf2 gene encodes a glycine-rich protein in mitochondrial; replacement of isoleucine by threonine at amino acid 78 of the RF2 protein causes functional loss of the rf2 allele. Moreover, CW-CMS is reported to be restored by a single recessive gene (Rf17) which is a retrograde-regulated male sterility (rms) gene (Table 2) [20].
\nS. No. | \n\nRf genes\n | \nLocality | \nMarker | \nCMS system | \nRestorer line | \nCausative gene | \nEncoded product | \nReference | \n
---|---|---|---|---|---|---|---|---|
1 | \n\nRf1a, Rf1b\n | \nChr-10 | \nInDel-Rf1a | \nCMS-BT | \nBTR, IR24, MTC10R; C 9083 | \nPPR8–1, PPR791,Rf1A, Rf1B\n | \nPPR | \n[13] | \n
2 | \n\nRf2\n | \nChr-2 | \nCAPS42–1 | \nCMS-LD | \nKasalath, Minghui 63 | \nLOC_Os02g17380.1 | \nGly. Rich protein | \n[14] | \n
3 | \n\nRf3\n | \nChr-1 | \nDRRM-Rf3–10 | \nCMS-WA | \nSwarna, PUSA 33 | \n— | \nPPR | \n[15] | \n
4 | \n\nRf4\n | \nChr-10 | \nRM6100 | \nCMS-WA | \nIR 24, Pusa 33, CRL 22R | \nPPR782a | \nPPR | \n[15] | \n
5 | \n\nRf5(t)\n | \nChr-10 | \nRM3150 | \nCMS-HL | \nMilyang 23 | \nPPR791 | \nPPR | \n[16] | \n
6 | \n\nRf6\n | \nChr-10 & 8 | \nRM5373 | \nCMS-HL | \n— | \n— | \n— | \n[16] | \n
7 | \n\nRf17\n | \nChr-4 | \nAT10.5–1, SNP 7–16 | \nCMS-CW | \nCWR | \nPPR2 | \nRNA interference | \n[17] | \n
8 | \n\nRf98\n | \nChr-10 | \nUK | \nCMS-RT98A | \nRT98C | \nPPR762 | \nPPR | \n[18] | \n
9 | \n\nRf102\n | \nChr-12 | \nUN | \nCMS-RT102A | \nRT102C, K102-Oryza rufipogon. T\n | \nUK | \nUK | \n[19] | \n
Restorer genes in rice plants.
Commercial hybrid seed production in rice where natural out-crossing (ranged only 0.3–3.0%) is very low, cumbersome, and an expansive task. To be practical and readily adoptable, it requires some specific parental requirements and agro-management practices. Invention of male sterile lines thus provided unique opportunity to start with the technology in rice. Based on mechanism of male sterility, threshold nature in male sterility expression and number of parental lines used, three types of hybrid seed production system namely three-line system (involving three parents, A, B, and R), two-line system (two parents, A and R), and one-line system (apomictic-based) exist. Among them, CGMS-based three-line system is more suitable, hence widely utilized (>90% of world’s hybrids developed utilizing this) in hybrid rice varietal development and seed production.
\nThis system involves three parents such as male sterile line (A-line, cytoplasmic male sterile), B-line (maintainer), and R (restorer) lines and two steps in seed production, that is, CMS multiplication and hybrid seed production under strict isolation (spatial or temporal or physical barrier). Male sterile line (A-line), because of their eliminated manual emasculation needs, served as seed parent and facilitates large-scale seed production. A suitable CMS line to be utilized as seed parent should have complete and stable male sterility, substantial seed producibility, wide compatibility, and good combining ability with minimum CMS load. The wealthy panicle and narrow semi-erect leaf configuration in seed parent has additional impact, assures more seed production. In Indian perspective, hybrid seed production is a major dilemma, generally keen to Rabi season, hence, CMS lines should have substantial cold tolerance at seedling stage and heat at flowering stage.
\nThe maintainer (B-line), on the other hand, is an isogenic to the CMS line (differs only for fertility/sterility) in their genetic constitution, able to produce functional pollen and maintain the sterility in male sterile line/seed parent. The maintainer line can maintain 100% male sterility in seed parent thus utilized to perpetuate CMS with their inherent male sterile ability.
\nIn contrast, restorer line can restore male fertility in F1s produced on male sterile parent, thus utilized as pollen parent in hybrid seed production. A good restorer should have substantial genetic distance with seed parent which is prerequisite and major determinant of the extent of heterosis in hybrids (more genetic distance more heterosis and vice-versa). Restorer is the major contributor of heterosis in three-line hybrids, hence, should have good combining, strong fertility restoration ability (dominant Rf gene(s) responsible for fertility restoration in CMS). Besides, restorer line with ideal plant type, acceptable grain quality parameters, substantial source-sink balance, heavy pollen load, and broad spectrum of resistance/tolerance against multiple biotic/abiotic stresses is imperative in maximization of genetic gain in hybrids.
\nThis system is a simple and more efficient hybrid breeding system in rice, involves only two parents, that is, A and R line in seed production, thus, referred as two-line system. This is a threshold of genetic male sterility (EGMS)-based hybrid rice breeding system, where male sterility is conditioned in specific environmental regimes such as long photoperiod (>13.5 h day length) and at elevated temperature (>30°C). In this system, male sterile parents are to be maintained by selfing under favorable conditions (below critical sterility point, i.e., <30°C temperature and at below CSP of photoperiod length, <12.5 h.).
\nTwo-line hybrid seed production system is an easy and effective alternative to CMS and has specific advantages as it requires only one step for seed production. In this system, any good combiner genotype irrespective of their fertility restoration ability can be utilized as a pollen parent. EGMS system is normal and does not exert any ill effect in the growth and development of carrier plant, and thus, exploits comparatively higher extent of heterosis (up to 5–10%) in F1 than the CGMS-based three-line system. The EGMS traits are governed by major genes, thus are easily transferable to any genetic background; besides, no CMS load could be helpful in reducing the potential vulnerability among the hybrids. Because of its eliminating needs for restorer genes in the male parents, this is ideal for developing inter-subspecific (indica/japonica) hybrids.
\nIn this system, seeds of rice hybrid once generated need not to be further produced in the hybrid seed production plot. This system is solely based on apomixes phenomenon (embryo developed apart from mixing of sexual gametes/fertilization) where the embryo developed without fertilization. In this system, hybrid seeds once generated will be maintained through apomixes in their original heterozygous form. The apomictic embryo is formed in the ovule via two fundamentally different pathways, sporophytic or gametophytic, which define the origin of the apomictic embryo [21]. In sporophytic apomixes, the embryo arises directly from the nucellus or the integument of the ovule in a process generally called adventitious embryony. In gametophytic apomixis, two mechanisms are generally recognized, diplospory and apospory. In both of these, an embryo sac is formed and the two mechanisms are distinguished by the origin of the cells that give rise to the apomictic embryo sac. In diplospory, the embryo sac originates from megaspore mother cells either directly by mitosis and/or after interrupted meiosis. In apospory, the embryo sac originates from nucellar cells. In both gametophytic mechanisms, the resulting nuclei forming the embryo sac are of the same ploidy as those found in the female parent because the reduction division cycle of meiosis does not occur. The embryo arises autonomously from one of the cells in the embryo sac.
\nIn a recent adventure, Delphine et al. reported three genes such as SPO11–1, REC8, and OSD1 in the sexual model plant Arabidopsis thaliana, which were combiningly mutated to turn meiosis into mitosis and its nourishing tissue from the female gametophyte without contribution of a male genome. This results in the production of clonal male and female gametes, but leads to doubling of ploidy at each generation when self-fertilized. Crossing a MiMe plant as male or female with a line whose genome is eliminated following fertilization (lines expressing modified CENH3) leads to the production of clonal offspring [22]. The MiMe technology was also implemented in rice to get diploid gametes. Furthermore, a study was conducted by Reda et al. to induce apomixis and fix heterosis in the sterile Egyptian Hybrid1 line using 0.2% colchicines [23]. It was observed that as colchicine is an alkaloid, which during cell division binds to tubulin protein of the spindle fiber and stops microtubules formation, and during meiosis, it prevents chromatids separation and inhibits cytokinesis. So ultimately, colchicines lead to meiosis aberrations, which produce aberrant microspores, pollen sterility, ovule sterility, as well as loss of fertility. Recently, a strategy based on the advanced technique, that is, CRISPR/Cas 9, has been utilized to introduce apomixis into rice (Oryza sativa) by mutating the three combined genes OsSPO11-1, OsREC8, OsOSD1, and OsMATL to get a MiMe phenotype [24].
\nHybrid technology is one of the greatest innovations in the modern era, contributed greatly in yield enhancement in several important crops. Over the decades of rigorous research, Chinese could develop parental lines, that is, cytoplasmic male-sterile line, maintainer line, and restorer line which assisted in the realization of heterosis exploitation in rice. Subsequently, hybrid seed production system was refined and world’s first hybrid rice was released for commercial cultivation during 1974 AD. The first generation wild abortive CMS line, that is, Zhenshan 97A was widely utilized and several elite hybrid rice varieties were commercialized. Besides, several CMS with altered genetic mechanism of male sterility expression were also identified and characterized.
\nAt beginning, low seed producibility with WA-CMS was a concern for its commercialization. However, with the keen interest of agronomist, management practices for hybrid seed production were sustainably rationalized. The Chinese government has supported this venture in pilot mode and established large and effective hybrid rice seed businesses in the late 1970s at all levels. Besides, intensive mechanization of hybrid seed production helped in modification of planting ratio (2R: A as 6–8 rows to 40–80 rows) and reducing the cost of production. Therefore, China could achieve seed yield by 2.7–3.0 t/ha on a large scale in hybrid rice seed production, which is further enhanced to 3400 kg/ha and maximizes their acreage.
\nOver past three decades, hybrid rice varieties have been substantial for national food security in the China which accounted for approximately 57% of the total 30-million-hectare rice planting area. The Ministry of Agriculture, China, has launched project on super hybrid rice development during 1996 which resulted altogether 73 super hybrids (52 three-line hybrids and 21 two-line hybrids) for commercial cultivation. Super hybrid P64S/E32 released recently has recorded new height of yield potential of17.1 t/ha with some striking characteristics [25].
\nBeside China, this technology has also been introduced and promoted by more than 40 countries around the world. At beginning, IRRI helped technically and supplied prerequisite parental materials. Later, most of the countries could establish their own hybrid rice breeding program and developed several heterotic hybrids. India was the second country after China that adopted this technology in 1989 and made substantial progress. At present, hybrid rice covers around 3.0 mha in India that has 6.8% of total rice area. Vietnam was the next to adopt this technology in 1992, harnessing yield of 6.3–6.8 t/ha from 0.7 mha, which covers around 10% of their rice area. In Philippines, it was introduced in 1993. Several popular hybrids like Magat, Mestizo, Mestizo 2, Mestizo 3, Bigante, Magilla, SL8H, Rizalina 28, etc. were developed and commercialized. Hybrid seed production in Philippines has been handled by “seed growers” cooperatives that are to produce around 60–70%. In Bangladesh, several rice hybrids were introduced and commercialized from China, India, and Philippines. They are almost self-sufficient in hybrid seed production, producing around 8000 tons to cover about 800,000 ha. In order, Indonesia also has substantial hybrid rice area, developed several good rice hybrids like Hipa7, Hipa 8, Hipa9, Hipa10, Hipa11, Hipa12 SBU, Hipa13, Hipa14 SBU, Hipa Jatim1, Hipa Jatim2 and Hipa Jatim3 were extensively commercialized, having yield superiority of 0.7–1.5 tons/ha over the lowland inbred varieties.
\nUSA has adopted this technology during 2000 and has developed and commercialized several two-line and three-line hybrids. Most of the hybrid rice cultivars in USA employed Clearfield (CL) technology offering selective control of weedy red rice. Rice hybrids, viz., Clearfield XL729, Clearfield XL745, Clearfield XP756 (a late maturing) and Clearfield XP4534 (new plant type) has shown yield advantage ranging from 16 to 39% over inbred cultivars are being commercialized by RiceTec.
\nIn India, systematic hybrid rice research was initiated in 1989.The first hybrid rice was released in Andhra Pradesh during 1993–1994 and India became the second country after China to commercialize hybrid rice. India has made substantial progress and developed total 117 (indica/indica) rice hybrids having 15–20% yield superiority with 115–150 days duration for various rice ecosystems. Recently, Savannah Private Limited from India has made another landmark by developing two two-line rice hybrids, viz., SAVA-124and SAVA-134, for commercial cultivation. In addition, more than 100 CMS in diversified genetic and cytoplasmic backgrounds have been developed and utilized. Among, the promising CMS lines CRMS 31A, CRMS 32A, CRMS 8A, PMS10A, PMS 17A, APMS 6A, DR8A, PUSA 5A, PUSA6A, RTN 12A, etc. are substantially being utilized in development of rice hybrids in India and abroad. Notably, medium-duration seedling stage cold-tolerant CMS, CRMS 32A, developed at NRRI under Kalinga-I cytoplasm is more suitable for development of hybrids for boro ecosystem. Two popular hybrid rice varieties, namely, Rajalaxmi and KRH 4 were developed using CRMS 32A as one among the parent.
\nHybrids released in India having unambiguous specificity like specific to ecosystem, tolerant to several abiotic/biotic stresses and consumer preferences (Table 3). These hybrid varieties can be utilized to up scale the hybrid rice cultivation and productivity enhancement per se in the respective area.
\nS. No. | \nStress | \nPromising hybrids | \n
---|---|---|
1 | \nRain-fed upland | \nDRRH-2, Pant Sankar Dhan-1, Pant Sankar Dhan-3, and KJTRH-4 | \n
2 | \nSalinity | \nDRRH-28, Pant Sankar Dhan-3, KRH-2, HRI-148, JRH-8, PHB-71, and Rajalaxmi | \n
3 | \nAlkalinity | \nSuruchi, PHB-71, JKRH-2000, CRHR-5, DRRH-2, DRRH-44, and Rajalaxmi | \n
4 | \n\nBoro/Summer season | \nRajalaxmi, CRHR-4, CRHR-32, NPH 924–1, PA 6444, Sahyadri, and KRH 2 | \n
5 | \nBB resistant | \nBS 6444G, Arize Prima, Rajalaxmi, Ajay, CR Dhan 701, PRH 10, etc. | \n
Rice hybrids tolerant to various stresses.
Hybrids like CRHR 105, CRHR 106, 25P25, 27P31 are suitable for high-temperature regime which has a more deleterious effect on seed development in hybrids. The hybrid varieties, US 382, Indam 200–17, US 312, DRRH3, and JKRH 401 having high N use efficiency are thus found suitable for cultivation in N-deficient soil. Besides, hybrids PNPH 24, RH 1531, and Arize Tej are under mid-early maturity group which can sustain substantially under drought situations. The problems of coastal and shallow lowland ecosystem sharing around 32% of total rice area can be addressed by adopting long-duration hybrids like CRHR 32, Arize Dhani, CRHR 34, CRHR 102, and Sahyadri 5 (Table 4).
\nAerobic condition | \nPSD 3, PSD 1, Rajalaxmi, Ajay, ADTRH 1, PRH 122, DRRH 44, HRI 126, JKRH 3333, and KRH 2 | \n
Early duration | \nCRHR 105, CRHR 106, 25P25, 27P31 (heat-tolerant), US 382, Indam 200–17, US 312`, DRRH3, JKRH 401high N use efficient; PNPH 24 and RH 1531, Arize Tej-mid-early drought-tolerant; DRRH2, and KJTRH-4 (upland) | \n
Long duration | \nCRHR 32, CRHR 34, CRHR 100, and Sahyadri 5 | \n
SRI | \nTNRH CO-4, KRH 4 | \n
Idly making | \nVNR 2355+ | \n
MS grains | \nCRHR 32, DRRH 3, 27P63, 25P25, and Suruchi | \n
Aromatic | \nPRH 122 (slight aroma), PRH 10 | \n
Hybrids suitable for specific condition.
The ICAR-National Rice Research Institute, Cuttack has been pioneer to start with the technology in late of seventh decade of last century, quite before the beginning of their project mode program in 1989 by ICAR. In the beginning, ICAR-NRRI has acquired all the prerequisite materials (CMS lines, viz., V 20A, Yar Ai Zhao A, Wu10A, MS 577A, Pankhari 203A, V 41A, Er-Jiu nanA, respective maintainers, nine other maintainers, and 13 restorers) from the IRRI (NRRI annual report 1981–1982). Systematic hybrid rice breeding was initiated in an interdisciplinary mode with objectives to develop desirable parental lines, viz., cytoplasmic genetic male sterile (CGMS) lines, maintainers, and restorers for the development of rice hybrids for irrigated and shallow submergence. The farmers in the rain fed shallow lowland ecosystem would be extremely benefited if the hybrid rice technology can be extended to this ecosystem, which need hybrids of Swarna duration. Keeping in views, ICAR-NRRI has developed three rice hybrids, viz., Ajay, Rajalaxmi, and CR Dhan 701 for this fragile ecosystem. Among them CR Dhan 701 is the country’s first long-duration hybrid, substitute for popular variety Swarna. Besides, NRRI has developed several promising CMS lines which have stable male sterility (WA, Kalinga-I and O. perennis, etc. cytoplasmic background), maintainers, and effective restorers. More than 45 CMS lines in diverse genetic and cytoplasmic backgrounds have been developed among Sarasa A, Pusa 33A (WA), Annada A (WA), Kiran A (WA), Deepa A (WA), Manipuri A (WA), Moti A (WA), Krishna A (O. perennis), Krishna A (Kalinga I), Mirai (Kalinga I), Padmini A, PS 92A and Sahabhagidhan A, etc., which are more prominent to be utilized in hybrid development. The medium-duration CMS, CRMS 31A (WA) and CRMS 32A (Kalinga-I) are significantly utilized for hybrid development at NRRI and elsewhere in the country. The CRMS 24A and CRMS 40A, developed under the nucleus background of Moti and Padmini are found suitable for late-duration hybrid breeding. Moreover, short-duration CMS, CRMS 8A, CRMS 51A and CRMS 52A and CRMS 53A having drought tolerance are also being used for development of hybrids for drought prone ecosystem.
\nThe latest release CR Dhan 701 (CRHR32) found suitable for irrigated-shallow lowland of Bihar, Gujarat and Odisha having MS grain type with an average yield capacity of 7.5 t/ha. This hybrid shows substantial tolerance to low light intensity, thus having great scope in eastern Indian states where low light limits the potential expression of hybrids/varieties during wet season. Moreover, hybrid Rajalaxmi (125–130 days) was developed utilizing native CMS line CRMS 32A, released by SVRC 2006/CVRC 2010 for irrigated-shallow lowland of Odisha and boro ecosystem of Odisha and Assam as it has seedling stage cold tolerance. Ajay is a medium-duration, long slender grain-type hybrid, released for cultivation in irrigated-shallow lowland of Odisha. As these hybrids are adaptable for eastern Indian climatic condition with assured remuneration, 12 private seed agencies over five states have commercialized them.
\nTo make this technology more sustainable and amenable to farmers, trait development strategy among the parental lines becomes mandatory. The parents of ICAR-NRRI bred hybrids Ajay, Rajalaxmi and CR Dhan 701 has been improved for bacterial blight, the most devastating disease of rice [26]. The submergence and salinity are the major abiotic stresses occur frequently in rain-fed shallow lowland area and causes substantial yield loss in rice. Hence, to cope up with the problems, and make hybrid rice more sustainable during these adversity, ICAR-NRRI has successfully stacked submergence and salinity-tolerant QTLs in the seed parents CRMS 31A and CRMS 32A. To enhance the seed producibility in seed parents, introgression of stigma exsertion trait from O. longistaminata into CRMS 31A and CRMS 32A, are under progress. To excavate the genetic region responding heterosis in rice, transcriptomic analysis of hybrids Rajalaxmi and Ajay are completed and interpreted. Availability of restorers for WA-CMS lines is very stumpy in nature, only 15% of total rice genotypes having the ability to restore complete fertility in WA-CMS-based hybrid rice [15]. Hence, good combiner genotypes having partial fertility restorers Mahalaxmi and Gayatri were improved by introgressing fertility restorer gene(s) Rf3 and Rf4 through MABB approach. Further, to make clear cut identity and ensure pure seed of parents/hybrids to the stack-holder, 12 signature markers that unambiguously distinguish 32 rice hybrids were developed, which can be utilized for DNA fingerprinting and genetic purity testing of hybrids.
\nRecent advancement in molecular biology has offered tremendous opportunities to the breeder and breeding per se in enhancement in their efficacy and speed up the varietal development process. It has diverse applications like mapping, tagging, amplification-based cloning, gene pyramiding, marker-assisted selection (MAS/MARS), fingerprinting applications, including varietal identification, ensuring seed purity, phylogeny and evolution studies, diversity analysis, and elimination of germplasm duplication. The progress in research related to application of DNA marker technology in hybrid rice improvement may be valuable in following way.
\nVarietal identity of hybrids and parents is imperative to assure the ownership (IPR issue) and pure seeds to the stakeholders. The genetic purity testing of hybrid seed is done by conducting Grow-Out-Test (GOT) which is time taking (needs one full growing season), tedious and very expensive. Molecular markers in this context found to be a suitable alternative, provide an unbiased means of identifying crop varieties. Among available DNA-based markers, sequence-tagged microsatellites (STMSs), which are co-dominant in nature, are widely used for speedy genetic purity assessment of the hybrids and parental lines [27, 28]. Besides, ICAR-NRRI has developed another set of nine signature markers which can distinguish parents CRMS 31A, CRMS 32A; and hybrids Ajay, Rajalaxmi and CR Dhan 701, unambiguously.
\nHybrid rice has been one of the innovations that led the quantum jump in rice productivity last century. However, the challenge of meeting the increasing demand for rice and making hybrid more sustainable under impeding climatic changes, trait development in parental lines for ideal plant type with substantial yield, grain quality, and resistance/tolerance to multiple biotic and abiotic stresses is necessary. In this context, conventional breeding is more cumbersome, time taking and less précised. The advancement in molecular breeding techniques makes it convenient to improve the parents and hybrids for desirable traits with great precision. Marker-assisted selection/MABB has provided strong utensils for indirect selection/trace the trait of interest at any plant growth stage. The bacterial blight and blast are the two-major destructive diseases affecting rice plant at different growth stages and caused substantial yield loss. Resistant genes for BB diseases have been deployed successfully in popular hybrids like Rajalaxmi, Ajay [26], BS 6444G, PRH 10 [29], Shanyou 63, Guangzhan63-4S; seed parent of CR Dhan 701; restorers Minghui 63 and Mianhui 725 [5, 26], Zhonghui 8006 and Zhonghui 218, etc. The popular CMS line Rongfeng A, Pusa 6A female parent of popular basmati hybrids PRH 10, RGD-7S, and RGD-8S [30] were successfully stacked with blast and BB resistant gene(s). Besides, CRMS 31A and CRMS 32A were deployed with submergence and salinity tolerance QTLs (NRRI newsletter 2015). Grain and eating quality in hybrids are concerns which are addressed by stacking QTLs/genes for quality traits in parents. Zhenshan 97A seed parent of several hybrids in China has been stacked with QTLs of AC, GC and GT [31]. Efforts were made toward quality improvement of both the parental lines of popular indica hybrids, viz., Xieyou57, using marker-assisted selection for Wx locus [32]. Yield-enhancing QTLs, yld1.1 and yld2.1, from O. rufipogon to restorer “Ce64” [33] are successfully stacked. Hybrid sterility in inter-subspecific (indica/japonica) hybrids is reported to be effectively addressed by utilizing genome editing tool “CRISPR/Cas9” [34].
\nLimited availability of fertility restorer system in rice makes three-line system very selective and less heterotic. Rice genotypes have fertility restorer ability can only be utilized as pollen parent in three-line hybrid breeding. Identification of genetically compatible, well combining restorers is tedious process, involve laborious test cross generation and evaluation steps. However, prior information on fertility restorer genes in the pollen parent excludes test cross steps thus make it convenient for saving time of hybrid development. Plenty of co-segregating molecular markers (tightly linked or functional markers) for fertility restorer gene(s) having functional specificity to diverse CMS systems are available (Table 2). The genic/functional markers, RM6100 and DRRM Rf3–10 of restorer gene(s) Rf4 and Rf3, respectively, are widely utilized for screening the fertility restoration efficacy of unknown pollen parents for WA and lineage CMS well in advance [15].
\nHybrid sterility is common nuisance menacing breeder to exploiting heterosis in inter-subspecific (5–10% more heterosis) hybrids. Generally, indica × japonica hybrids are sterile due to lack of wide compatibility (WC) between parents. It is reported that hybrid sterility in inter-subspecific crosses is mainly affected by the genes at Sb, Sc, Sd, and Se [35] loci causes male sterility in F1and the gene at S5 locus cause female sterility in F1. Presence of these genic regions in at least one parent ensures complete fertility in resulting hybrids. These gene(s) can be assessed in advance by utilizing co-segregating markers (S5-InDel, functional marker to S5n) [36] and G02–14827 (genic marker) PSM8, PSM12, and PSM180 (linked SSR); IND19 and ID5 (indel markers) to Sb, Sc, Sd, and Se, loci). Thus, it helps breeder in selection of WC-positive parent in more predictable way which circumvents laborious test-cross and their evaluations steps.
\nGenetic distance and level of genetic gain/breeding value in parents are major determinants of extent of heterosis in the resulting hybrid. Molecular markers help in assessing the genetic diversity among parents and breeding values in progenies (through genomic selection, high-density SNP genotyping) with great convenient. There are abundant STMS and SNP markers available which can be utilized for assessment of genetic diversity/genetic distance between parents and genomic selection in progenies easily [37]. Hence, this is helpful in the selection of diverse parents with maximum breeding values in turn higher heterosis or genetic gain in hybrids.
\nThe extent of genetic variation and selection strategies are keys to the success of heterosis breeding. Accurate assessment and assignment of parental lines into heterotic groups “group of genotypes (related or unrelated) having similar combing ability and heterosis response when crossed with the genotypes of other diverse group” are fundamental prerequisites. Usually it is evaluated by combining ability analysis of parents and hybrids in multi-environment trials. However, advances in molecular marker technology have made it possible to combine information on parental pedigree and field trials with molecular marker data to detect and establish heterotic groups. Several heterotic groups have been developed and utilized for three-line and two-line hybrid development in rice [38].
\nOmics techniques reported to have great potential in excavation of QTLs/gene(s) responses heterosis in rice. By utilizing genomics tools, many QTLs/genes for several important traits has been mapped, validated, and deployed in trait development in rice. The transcriptomics, an emerging technique helps in genome-scale comparisons of the transcripts of different individuals within the same species/population. It helps in understanding the level of variation for gene expression, as measured by transcript abundance that exists within plant species and between hybrids and their parents. This is useful for identification of transcript and gene per se involves in heterotic expression. Moreover, epigenetics, a posttranslational biochemical regulation of gene is found to be playing substantial role in trait expression. Individuals of the same species can have epigenetic variation in addition to genome and transcriptome content variation. A potential role for epigenetic regulation in heterosis has been proposed. It is possible for epigenetic variation to affect heterosis by creating stable epialleles that would behave similarly to the genomic or transcriptomic differences. Alternatively, hybrids may exhibit unique epigenomic states that lead to heterosis.
\nDespite of being remunerative and varietal abundancy, HR technology could not make substantial dent in the rice farming system outside China. The following are the inherited void led poor acceptability and acreage expansion of hybrids:
\nOutside China, WA-CMS or their lineages are commonly utilized as seed parent in more than 90%rice hybrids. Several alternative MS cytoplasmic sources such as BT-CMS, HL-CMS, and CW-CMS are identified in China, but the hybrid breeding program of other countries relied only on WA-CMS which has several inherited abnormalities. These narrowed genetics of sterile cytoplasm limits the extent heterosis exploitation and make hybrids vulnerable to many biotic and abiotic stresses.
\nTwo-lines and inter-subspecific (indica/japonica) hybrids are comparatively more heterotic (5–10%) than three-line indica hybrids. But owing to several inevitable difficulties in seed production of two-line hybrids and poor grain and eating quality in inter-subspecific hybrids, both could not be exploited in the countries like India who has vast climatic and food affection diversity. We are utilizing three-line indica hybrids which are comparatively less heterotic hybrid breeding systems giving low yields. Hence, focused and intensive research is proposed to make above said hitches be addressed in future.
\nIn hybrids, consumable parts are F2 grains, segregating for various quality traits hence very poor in quality limits its acceptability among stakeholders. Therefore, make hybrids more sustainable and popular, quality traits in hybrids needs to be addressed urgently in the country like India where people have vast category of food fondness. Hence, a strong breeding strategy for quality concern in hybrids is needs to be devised and implemented.
\nAlthough heterosis, or hybrid vigor, is widely exploited in agriculture, but despite extensive investigation, complete description of its molecular underpinnings has remained elusive. It appears that there is not a single, simple explanation for heterosis. Instead, it is likely that heterosis arises in crosses between genetically distinct individuals because of a diversity of mechanisms. Hence, mining factors responding heterosis in rice will have a substantial role in development and exploiting heterosis in most precise way.
\nHybrid sterility is key nuisance in inter-subspecific hybrids, limiting development and commercialization of more heterotic indica/japonica hybrid in rice. The sterility in hybrids (inter-subspecific) generally occurs due to non-functional pollens as well as sterility in female reproductive organs. It is reported that mutant of S-i alleles at Sb, Sc, Sd, and Se loci produce sterile pollens; and mutants of S5locus causes sterility in female gamete. Hence, trait development for wide compatibility in either parent has great opportunity in addressing the hybrid sterility in rice.
\nInter-subspecific (indica/japonica) hybrids as discussed in earlier section are more heterotic than intra-subspecific hybrids. However, owing to hybrid sterility and poor grain quality, this genetic pool remains untapped. Grain quality of inter-subspecific hybrids proposed to be improved by utilizing parental combinations having good combining ability but similar in quality parameters, might reduce the concern of segregation for quality traits. Hybrid sterility problem in inter-subspecific hybrids can be addressed by stacking indica allele (S-i) at Sb, Sc, Sd, and Se loci and the neutral allele (S-n) at S5locusin to japonica genetic background [35] or by silencing the S-i and S5 mutant loci through genome editing tools [34].
\nIn three-line hybrid system, cytoplasm of CMS exerts various unwanted effect (called CMS penalty) and reduces the complete heterosis expression (up to 5–10%) in CGMS hybrids. Iso-cytoplasmic restorer is fertile transgressive segregant of CGMS hybrid, having same cytoplasm as of CMS. In combination with iso-cyto-CMS, it can normalize the fatal cyto-nuclear conflicts, hence enhances the heterosis to substantial extent. In rice, several iso-cytoplasmic restorers has been developed and utilized in hybrid rice research [39].
\nLow seed producibility (1.5–2.5 t/ha) in the CMS remains a concern, restricts seed abundancy, and area expansion in India. Trait development in seed parent for out-crossing traits like stigma exertion, complete panicle exertion is important and needs to be addressed strategically. Recently, a CMS line, IR-79156A possessing more than 50% out-crossing, developed by IRRI showed seed producibility of 3.5 t/ha.
\nTo maximize genetic gain in rice, breeding of ideal plant type was started long back in Japan and subsequently adopted by China. Through morphological improvement and adopting inter-subspecific (indica/japonica) hybrid strategies, substantial progress in ideotype hybrid breeding “super hybrid” have been achieved. China, indeed has made considerable progress and released more than 100 high yielding super hybrids [25]. Hence, inclusion of inter-subspecific quality type inbreds “super rice” in hybrid development will have substantial impact in attaining quantum genetic gains in hybrids.
\nInspite of being more cumbersome and high input intense practice, hybrid rice seed production is a profitable venture. It creates additional job opportunity (requires 100–105 more-man days) and provides more net income (around 1050 USD/ha net income, 70% more than the unit production cost) as compared to seed production of HYV (192.0 USD/ha, only 18% more than production cost) (Table 5). The market price of hybrid seed is 3.5–4.25 USD per kg. The farmers producing the hybrid seed get only 1.15–1.30 USD per kg. In case of low production (<5 quintal/acre) farmers get minimum 635.0 USD as compensation from seed production agencies.
\nItem | \nQuantity/number (per hectare) | \nCost/income (USD) | \n||
---|---|---|---|---|
Hybrid seed | \nHYV | \n|||
Seed cost | \nMale | \n5 kg @ 0.71 USD/kg | \n4 | \n28 | \n
Female | \n15 kg @ 5.65 USD/kg | \n42 | \nNil | \n|
Labor cost | \n250/145 @ 2.83 USD/labor/day | \n707 | \n410 | \n|
FYM and fertilizer cost | \nN:P:K (100:50:50) (based on market price) | \n76 | \n76 | \n|
Irrigation | \n18–20 Irrigation (weekly) @ 21.20USD/ha/irrigation | \n425 | \n425 | \n|
Gibberellic acid | \n\n | 28 | \nNil | \n|
Others | \n\n | 212 | \n141 | \n|
Total cost | \n\n | 1494 | \n1080 | \n|
Average production | \n\n | 2.0 t/ha | \n4.5 | \n|
Gross income | \nPrice @ 1.27USD/kg and 0.28USD/kg\na\n\n | \n2544 | \n1272 | \n|
Net income | \n\n | 1050 | \n192 | \n
Cost analysis of hybrid rice seed.
Price of seed is the price given to the farmer.
Source: Verma et al., [40].
Hybrid technology has been substantial in enhancement of rice productivity per se production in temperate countries, however, owing to low photo-intensity during growing period in tropics, its impact remains meager. Under changing climatic and agriculture scenario, rice hybrid is likely to face stiff competition to sustain in future. Despite having great potential to enhance production and productivity, it has not been adopted on large scale as was expected. This is due to several constraints like lack of acceptability of hybrids in some regions such as Southern India due to region-specific grain quality requirement. Moderate (15–20%) yield advantage in hybrids is not economically very attractive and there is a need to increase the magnitude of heterosis further. Lower market price offered for the hybrid rice produce by millers/trader sis acting as a deterrent for many farmers to take up hybrid rice cultivation. Higher seed cost is another restrain for large-scale adoption and hence there is a need to enhance the seed yield in hybrid rice seed production plots. Efforts for creating awareness and for technology transfer were inadequate in initial stages. Involvement of public sector seed corporations in large-scale seed production has been less than expected. Hybrid rice for aerobic/upland, boro season and long-duration hybrids for shallow lowland conditions are to be developed. Most of the constraints mentioned above are being addressed with right earnestness through the ongoing research projects and transfer of technology efforts.
\nSince inception, this technology has a substantial impact in enhancing the productivity and production in crop plant and livelihood of the farming community. In rice, it is adopted worldwide over 40 countries; however, it could not make a substantial dent in outside of China. This chapter has represented the holistic status of hybrid technology in rice along with future research and developmental road map to make this venture more substantial and sustainable for benefiting all stakeholder involves. This chapter identifies the ambiguities held responsible for slow adoption of this technology and probable strategies to get rid of those. Therefore, this chapter will be helpful for researchers and students in planning of future hybrid rice breeding strategies.
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Today his focus is on defining the growth and development strategy for the company.",institutionString:null,institution:{name:"TU Wien",country:{name:"Austria"}}},{id:"19816",title:"Prof.",name:"Alexander",middleName:null,surname:"Kokorin",slug:"alexander-kokorin",fullName:"Alexander Kokorin",position:null,profilePictureURL:"https://mts.intechopen.com/storage/users/19816/images/1607_n.jpg",biography:"Alexander I. Kokorin: born: 1947, Moscow; DSc., PhD; Principal Research Fellow (Research Professor) of Department of Kinetics and Catalysis, N. Semenov Institute of Chemical Physics, Russian Academy of Sciences, Moscow.\r\nArea of research interests: physical chemistry of complex-organized molecular and nanosized systems, including polymer-metal complexes; the surface of doped oxide semiconductors. 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