\r\n\tIt is believed that deterioration in structures are needed to be linked with risk management in construction. Faulty of construction directly affect to the deterioration. Therefore, second part of this book considers the lessons learned in construction management. Project and site managers, quality engineers are most welcome to discuss the reasons of deteriorated structures through project planning to the serviceability of such structures.
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Taylor at the Midvale Steel Company in the 1880s as he progressed from machinist, to time clerk, to machine shop foreman, ultimately becoming chief engineer upon receiving a mechanical engineering degree in 1883. His participation in the American Society of Mechanical Engineers (ASME) provided him with the opportunity to present his shop management practices which were referred to as “work measurement” when applied to a specific work task (manual labor such as shoveling; skilled labor such as lathe operation). Broader applications to groups of workers in a plant or service organization (educational organizations, government agencies, the ASME) became known world-wide as Scientific Management [1], especially after Taylor testified before the US Interstate Commerce Commission in 1911.
Henry L. Gantt was recruited to perform work measurement at Midvale Steel under Taylor’s guidance, and as a consultant one speed and feed problems in metal cutting at Bethlehem Steel. Gantt modified one of Taylor’s published practices (piece-rate system) to account for productivity factors outside the workers control. Gantt became an independent consultant and ultimately lectured on IE at four US universities. Another early practitioner of IE was Morris L. Cooke, whom Taylor funded to work on efficiency and effectiveness of the ASME, the Carnegie Foundation, and the municipal government of Philadelphia. Frank B. Gilbreth originated the practice of work measurement in the construction trades, though he never attended college. His approach came to be known as time and motion study, which he first applied to bricklaying (a trade he learned as an apprentice). He insisted on division of labor between the brick mason (skilled labor) and the unskilled workers who “set up” the mason with bricks and fresh mortar; the specific location of the bricks and mortar relative to the mason, and even the consistency of the mortar, could be planned to make the mason as productive as possible. Furthermore, with appropriate design of the motions the mason should use, he demonstrated that the mason could increase the number of bricks laid in a given time by a factor of three. At age 27, Gilbreth founded (1895) a highly successful construction firm wherein all work was designed using time and motion study, but gave it up at age 44 to become a full-time management consultant. Frank’s wife, Lillian M. Gilbreth, was a PhD psychologist who assisted Frank in the preparation of six books between 1908 and 1917 to disseminate what he had learned about the broad topic of performance measurement, starting with the worker and broadening to the work processes and the overall work system.
As Japan began to recover from destruction of its industrial base during WWII, and to transition from essentially an agrarian society to an economic powerhouse, their industrial/production engineers originated many practices now considered part of modern industrial engineering. Starting in the 1970s and intensifying in the 1980s, there was significant debate in the US and other advanced economies in the West concerning what was enabling the Japanese to capture larger and larger market share in technological products such as automobiles, televisions, and copy machines. There was a US IE professor, Richard J. Schonberger, who spend a significant amount of time in Japan and authored several books [2, 3, 4] detailing his interviews and observations from visiting top-performing Japanese manufacturing firms. In Japanese Manufacturing Techniques [2], he revealed the following nine “hidden lessons in simplicity”:
Fewer suppliers
Reduced part counts
Focused factories (focus on a narrow line of products)
Scheduling to a rate, instead of scheduling by lots
Fewer racks on the plant floor
More frequent deliveries (in-plant moves, as well as deliveries from suppliers)
Smaller plants
Shorter distances, less reporting, less inspectors, less buffer stock
Fewer job classifications.
In World Class Manufacturing [3], Schonberger claimed production management in the US had become overly focused on “managing by the numbers” by which he meant measuring plant performance at too high a level (revenue, fixed and variable costs, profit) to really uncover hidden efficiency and quality effects; whereas in contrast, WCM mandates simplification and direct action—do it, judge it, measure it, diagnose it, fix it, manage it, on the factory floor. He provided a variety of examples with diagrams/photographs in [4], World Class Manufacturing Casebook. In [3] Schonberger observed that in 1980, the first US WCM thrusts followed two parallel paths: a quality path with a goal of zero defects known in Japan at Total Quality Control (TQC) and in the US as Total Quality Management (TQM); a just-in-time (JIT) productivity path, as a means of coping with high-variety, small lot, short lead-time production. JIT aims to have every operation make the needed items at the right time in the right quantities, at low cost. JIT pursues a goal of one-piece flow, small-lot production, with minimal inventory throughout the system. A third WCM practice which supports both TQC and JIT is known as Total Productive Maintenance (TPM) and will be described below when we introduce the metric Overall Equipment Effectiveness (OEE). The three practices are synergistic—for instance, JIT will fail if incoming part quality is not (nearly) perfect and processing equipment does not have OEE near 100%.
Most US industrial engineers first learned details of TPM through the 1988 English version of Nakajima’s TPM: Introduction to Total Productive Maintenance [5]. According to Nakajima “TPM is an innovative approach to maintenance that optimizes equipment effectiveness, eliminates breakdowns, and promotes autonomous operator maintenance through day-to-day activities involving the total workforce.” Seven years later, two North American practitioners Charles Robinson and Andrew Ginder produced the well-known Implementing TPM: The North American Experience [6] and therein defined TPM to be “a plant improvement methodology which enables continuous and rapid improvement of the manufacturing process the use of employee involvement, employee empowerment, and closed-loop measurement of results.” In the decade following Robinson and Ginder [6], publications on “TPM Practices and Cases” [7] and “Lean TPM” [8] appeared in the US and Great Britain. In the recent past, Ortiz contributed The TPM Playbook: A Step-by-Step Guideline for the Lean Practitioner [9] and Peng, in response with the digital revolution in production, published Equipment Maintenance in the Post-Maintenance Era: A New Alternative to Total Productive Maintenance (TPM) [10]. All of these references include a section or entire chapter explaining the measurement of Overall Equipment Effectiveness; furthermore, all suggest an engineer or improvement team could focus on OEE for a single machine (workstation), OEE for a production line or process, and OEE for the overall plant. Comparisons across shifts, days, months, etc. would detect improving or deteriorating performance. Furthermore, comparisons across similar machines, processes, or plants could be very useful to department, process, or plant managers.
OEE for a given machine, line, or plant is the product of availability, performance efficiency (processing rate ratioed with the design “ideal”), and quality rate (proportion of good products produced—the yield). Because each of these inputs is measured as a percentage, the closer OEE is to 100%, the better; world-class OEE is considered 85% or higher (some authors say 90% or higher). OEE is formally calculated using the following expressions, each expressed as a percentage:
The calculation of each of these quantities is illustrated by example in the references by Nakajima [5], and Robinson and Ginder [6]. The example in Nakajima further illustrates why the three input quantities to OEE are seldom calculated to be 100%. Essentially, the use of OEE in TPM uncovers the “Six Big Losses” which become the focus of improvement efforts by an individual engineer, or a team. The Six Big Losses are grouped as follows:
Losses that determine equipment availability
Equipment failure losses (requiring corrective maintenance)
Set-up and adjustment losses
Losses that determine performance efficiency
Idling and minor stoppages (e.g., clearing a jammed workpiece, or stopping for a visitor)
Reduced speed (e.g., running slower to avoid overheating, or avoid early job completion)
Losses that determine rate of quality products
Defects and rework
Reduced yield due to start-up losses (either due to nature of process, or company policy)
Some examples of how to improve OEE above status quo, based on the six big losses as numbered above, would be:
Study equipment failure and repair records. Use the Pareto Principle to identify which machines are causing downtime, in rank order: then, for the least available machine, identify the machine elements that are the causes of downtime, in rank order. Focus improvement efforts on the most problematic machines, and once identified, the most problematic machine elements.
To reduce set-up time, there is a Japanese practice originally known as Single Minute Change of Die (SMED)—meaning work to reduce change-over times to less than 10 minutes (single digits) with a goal of single minute change-overs; in the US, this practice is called Quick Changeover Technology and, for example, has been observed in casting machines in pipe shops, and welding machines for tubular steel products. This practice is essentially a specialized time and motion study, again carried out by a single engineer or improvement team, and the saving from avoided set-up losses can be substantial.
Periods of idling and instances of minor stoppages should be recorded (total time lost, situation and/or causes).
Reduced speed losses—there may be good reasons for running equipment at less than ideal processing rate, such as to avoid overstressing the equipment or safety concerns for the operator or other workers in the vicinity. In instances where work crews intentionally slow down, management needs to re-plan schedules so every worker can get in a full shift, having come to work intending to be paid for a full shift.
Defects and rework must be recorded and carefully examined to determine root causes, and then immediate corrective actions taken (standards modified or adjusted) to hopefully prevent the same problems in the future. Follow-up is critical by the engineer, manager, or team to verify the action installed is working and has become the standard.
Start-up losses may be unavoidable with the materials, machine, and set-up required; or, they may indicate a company policy that is outdated (current machine can now produce acceptable quality with first unit produced, or could with appropriate attention from engineering, maintenance, and production).
For more details on data collection and the calculation/application of OEE, see three references focused specifically on OEE: Muchiri and Pintelon’s 2008 article “Literature Review and Practical Application Discussion” [11]; Hansen’s Overall Equipment Effectiveness book [12]; and The OEE Primer: Understanding Overall Equipment Effectiveness, Reliability, and Maintainability [13] by Stamatis. As with the world-wide spread of Scientific Management, the use of OEE by industrial engineers has spread to practitioners in Europe (e.g., see an application in France to large-scale production of ductile iron pipe [14], and in Asia, for example, applications to sugar mills in India [15, 16]).
A simple definition of service is “work performed for someone else.” In other words, services are all those economic activities in which the primary output is neither a good nor a construct, so services are for the most part intangible. Of course, services may occur internal to a company, educational institution, medical facility, or government agency, or in service encounters between individuals, or exchanges between larger-scale entities—two companies, or perhaps a university and a government agency. In general, services cannot be inventoried. When considering services in context of the overall economy, a big distinction is that product-oriented sectors of an economy always produce a tangible product; a service may or may not terminate in a tangible product. Also, services are rendered on demand—either instant demand or scheduled demand—often with the customer present and involved in the service. So, the reliability characteristic “ready on demand” is critical to high quality service. Once service begins, uninterrupted service may be another customer expectation. Variability of service in response to specific customer requests may be intentional—information gets transformed into customized action in an attempt to satisfy the requests. It may also be unclear which party “owns” the service. In contrast, a manufactured product is tangible, produced and consumed at different locations at different times, expected to be of consistent quality, to be inventoried with like items, and to have clear ownership as it changes hands.
The Service Sector of the US economy in 2019 accounted for 79% of US employment. The percentage of service workers in other advanced economies are approximately 75% in Great Britain, 65% in France, and 60% in Germany and Japan. Service is considered a tertiary sector following the Primary Sector “Extractive” industries (Fishing, Agriculture, Mining, Oil and Gas, etc.) and the Secondary Sector “Transformative” industries (Manufacturing and Construction). The service sector is highly diverse; see the following groupings used by the US Dept. of Labor:
Trade, Transportation, and Utilities
Wholesale Trade (NAICS 42)
Retail Trade (NAICS 44-45)
Transportation and Warehousing (NAICS 48-49)
Utilities (NAICS 22)
Information (NAICS 51)
Financial Activities
Finance and Insurance (NAICS 52)
Real Estate and Rental and Leasing (NAICS 53)
Professional and Business Services
Professional Scientific and Technical Services (NAICS 54)
Management of Companies and Enterprises (NAICS 55)
Administrative and Support; Waste Management and Remediation (NAICS 56)
Education and Health Services
Educational Services (NAICS 61)
Health Care and Social Assistance (NAICS 62)
Leisure and Hospitality
Arts, Entertainment, and Recreation (NAICS 71)
Accommodations and Food Services (NAICS 72)
Other Services (except Public Administration) (NAICS 81)
Government
Characteristics of services are:
The product is intangible, for the most part
Usually performed in real time, with the customer present and often participating
Seldom inventoried, so must be delivered on the customer’s schedule
Something of value is provided (like manufacturing) but in a more immediate, personalized manner.
Quality of a product (service, good, or software) has been defined by Juran [17] as “fitness for use, in the intended environment” and by Deming [18] as “meets or exceeds customer expectations.” Therefore, a broad definition of service quality might be “fitness for use as determined by those features of the service that the customer considers to be beneficial.” As explained in Jain and Gupta [19], “services require a distinct framework for quality explication and measurement” and “involves evaluation of the outcome (i.e., what the customer actually receives from the service) and the process of service act (i.e., the manner in which the service is delivered).” Another line of research at that time concerned measurement of service expectations, pre- and post-consumption [20]. Parasuraman et al. [21] created the SERVQUAL scales and questionnaire organized around these five measures of service quality:
Reliability—the ability to perform the desired service dependably and accurately
Assurance—the knowledge and courtesy of employees and their ability to convey trust and confidence
Tangibles—the appearance of physical facilities, equipment, personnel, and communication materials
Empathy—the provision of caring, individualized attention to the customer
Responsiveness—the willingness to help customers and provide prompt service.
In a later publication [22], these same three authors presented a list of nine dimensions classifying how customers perceive service quality:
Tangibles—physical appearance
Reliability—performed as promised, consistently
Responsiveness
Competence
Credibility
Security/Safety
Access—easy to do business with
Communication—keeping customer informed
Understanding customer needs.
Pitt et al. [23] concluded that SERVQUAL is an appropriate instrument for researchers seeking a measure of information system service quality.
We have collected together six widely-known customer reactions to service quality:
Poor or inattentive service costs companies about 10% of volume annually (until corrected)
96% of unhappy customers never complain, but 90% never return. Each unhappy customer tells at least nine others.
Each happy customer tells five others, who may become future customers.
The best opportunity to increase sales and market share is through your present customer base
Customer perception of quality of service depends heavily on employee’s job satisfaction (dis-satisfaction)
Service personnel are critically dependent on systems (often computer-based) to deliver quality to the customer.
Let us consider several examples of the last point, which is very important for the industrial engineer:
A college instructor depends on:
The student registration system to provide accurate class rolls and a means to report final grades to the registrar
The classroom assignment system to provide a lecture hall to match the enrollment
The textbook ordering system to order, receive, and distribute the correct class materials in the correct quantities, on time
The classroom audio-visual system and computer software/internet access provided in the lecture hall.
A medical doctor seeing patients in his/her clinic depends on:
The patient appointment scheduling system
The measurement of patient vital signs by nurses as the visit begins, with computer access
Blood testing machines and/or radiological scans done prior to the visit, with computer access
Computer access to records of previous ailments and treatments, surgeries, vaccinations, etc.
Equipment he/she may use during the patient encounter.
A service representative at a cable television/internet provider depends on:
An information system showing the customer’s current service details, including start-up and service end dates
An information system showing additional or alternative services available to the customer based on location, with costs and time frame for change in service
A billing system should balances in accounts, due dates, penalties for late payments, etc.
A bank teller for customers who walk in the branch and queue for service, depends on:
An information system showing a customer’s accounts, safe deposit boxes, progress on any money electronically moved from or to customer’s accounts
An information system tracking cash transactions (deposits, dispersals, exchanges, etc.) completed by the teller and what should be the status of their cash drawer
In a large bank, a formal schedule of teller work assignments and for each, their schedule of breaks and lunch, and an out-of-office schedule for the current day and perhaps for the weeks or months ahead.
Overall Service Effectiveness (OSE) was first described in Berhan [24], and is the focus of the remainder of this chapter. The OSE metric for services extends the OEE production metric developed along with TPM as described earlier in the chapter. For the reader’s convenience, we shall demonstrate how OSE is a simple rewrite of the formulas for OEE and its three input components in a manner that fits service transactions an industrial engineer might be challenged to design or improve, using OSE as a guide.
In the equations below, the term “units” could be units of a manufactured good or quantities of a service completed. Examples of the latter might be: queries to an information systems; patients seen by a doctor or dentist; customer transactions at a bank—in person or electronic; riders transported by a bus or aircraft, or by the bus line or airline. Note these are all situations which an industrial engineer might encounter, and traditional IE tools such as queuing theory or system simulation might be in use. Agreeing with the OSE equations of Berhan [24], we shall use:
An example for an urban transportation system described in Berhan [24] adapted the equations for the three inputs above to the specifics of the service operation as follows:
Note that the bus service, like many encountered in modern society, is a “knowledge embedded service” [25] which are services which embed the customer value in a system that provides the service, so human-machine system reliability is a key component of the availability input to OSE for such services. Here, the driver’s knowledge of the route and how to operate the bus matters as much as the bus reliability.
Using real data from the public transport (bus) system in Addis Ababa, Ethiopia: Berhan first computed planned downtime (lunch breaks and shift changes), downtime and speed losses, performance efficiency losses, and finally quality and yield losses; Berhan then computed:
which yielded a system ‐ wide effectiveness measure of
showing this service system needs significant improvement in order to be rated “world-class”.
Just like in manufacturing, the OSE could also have been calculated for each bus individually, or for groups of busses that act together to cover a given route or sector within the city. Hence, OSE would be useful for service performance improvement at the bus, route, or (as demonstrated) system level.
This chapter provided background on the application of work measurement to services, starting with Taylor and his associates, and tracing the evolution from the plant performance metric Overall Equipment Effectiveness to an innovative service performance metric Overall Service Effectiveness (OSE). As illustrated in the analysis of an existing city bus system, the details used to compute the OSE inputs (availability, performance efficiency, quality rate) point toward actions that would improve OSE toward 100%. When designing a new service system (e.g., bus line, bank layout, fast food restaurant) the OSE metric can be used along with other industrial engineering tools (e.g., classic queuing formulas, systems simulation, engineering economy) to arrive at the most cost-effective layout, equipment/software, and staffing to handle forecast service demands.
The onset of leaf senescence is a highly regulated developmental program that is controlled by both genetics and the environment. Multiple stresses in plants induce programmed cell death, and the underlying regulatory mechanisms are often associated with molecular links of developmentally programmed senescence. The transcriptome changes induced by different environmental stressors are not entirely overlapping, but functional analysis of genes commonly induced as shared responses can give clues on signaling integration. This approach has been used to select for overlapping genes as candidate regulatory components that integrate the ER stress and osmotic stress responses, which were shown later to participate also in natural leaf senescence. Among genes identified as components of the ER and osmotic stress shared response, the developmental and cell death (DCD) domain-containing asparagine-rich proteins (NRP-A and NRP-B) were the first ones to be characterized as cell death-promoting proteins, and hence this multiple stress-integrating signaling was designated as stress-induced DCD/NRP-mediated cell death response. Further characterization of the cell death pathway implicated in the discovery of the signaling module ERD15/NRPs/GmNAC81:GmNAC30/VPE that also has been shown to operate in developmentally programmed leaf senescence. This plant-specific cell death signaling module, which operates in both stress-induced and natural leaf senescence, constitutes the primary focus of this chapter.
Organisms, in general, are continually adapting to internal and external stimuli, which activate sensor proteins to subsequently transmit the signal to downstream effectors responsible for the assembly of adaptive cellular responses [1]. Abiotic stresses consist of a set of adverse environmental conditions that limits plant development. Cold, high temperature, salinity, water availability (drought or overflow), radiation, pollution, and chemical exposure are the most common examples of types of abiotic stresses [2].
Generally, a signaling sensor network connects internal and external stimuli to adaptive responses leading to molecular modifications that allow physiological adjustments, which ultimately cause susceptibility or tolerance to the exposed conditions. Molecular responses to abiotic stress conditions in plants are crucial for survival and productivity as these stresses often limit yield. Among abiotic stresses, drought and excess salinity conditions induce sophisticated adaptive responses in plants to cope with or acclimate to these adverse environmental conditions [3, 4]. Some types of abiotic stress responses are better understood than others. In plants, for example, the molecular mechanisms of perception and responses to drought, high salinity, and endoplasmic reticulum stress are well characterized, and many stress-related cell signaling pathways are completely elucidated, revealing some convergence points between them.
The osmotic stress in plants, caused by water deprivation or high salinity, for example, undergoes a set of characteristic morphological, molecular, and physiological changes. One of the most notorious symptoms in plants under low water availability is the ABA-mediated stomatal closure [5]. This hormone-mediated morphological change affects plant physiology. The stomatal closure prevents the evapotranspiration, optimizing the cell water use, but it also compromises carbon dioxide uptake, causing imbalances on photosynthetic apparatus, which culminates on reactive oxygen species (ROS) production [6, 7]. The ROS accumulation acts as a signal to the cell, which triggers mechanisms of ROS-associated detoxification, including upregulation of antioxidant enzymes, osmolyte, and electron-carrier synthesis [8]. There is evidence that osmotic stress and temperature changes are capable of generating lipid-derived signal transducers, including the phosphatidic acid, phosphoinositides, sphingolipids, lysophospholipids, oxylipins, N-acylethanolamines, and others. Water deprivation causes a collapse on the organization of membrane lipids, disrupting its permeability and some significant molecular interactions between lipids and proteins, which act as a cell signal to stress-mediated physiological changes. The mechanisms of how stress responses are connected with membrane lipid transducer generation are still unclear, but lipid messengers can alter protein and enzymatic functions [9].
The endoplasmic reticulum is one of the most dynamics organelles in cell machinery. It is the gateway for the synthesis of secretory proteins and contains the necessary apparatus to ensure quality protein synthesis, protein maturation, and secretion in eukaryotic cells [10]. Furthermore, the ER can modulate some chronic stress-related pathways, promoting oxidative stress, autophagy, and apoptotic cell death in mammals and plant cells [11, 12, 13].
Several adverse environmental conditions can affect the ER quality control machinery, causing unfolded/misfolded protein accumulation in the ER lumen. The secretory proteins are synthesized in ER membrane-bound polysomes, and, as soon as they enter the organelle, they are processed by the ER processing machinery. Under normal conditions, there is a perfect balance between the rate of protein synthesis and ER processing capacity. Any conditions that disrupt this balance promote unfolded/misfolded protein accumulation in the ER lumen. As a consequence, the perturbation on ER function triggers a sophisticated and coordinated signal cascade, perceived by ER membrane-associated sensors, which activate the expression of ER-resident chaperones, foldases, and components of the ER quality control machinery. Collectively, these cytoprotective mechanisms are known as the unfolded protein response pathway (UPR, Figure 1) [14].
The endoplasmic reticulum stress response in Arabidopsis. The secretory proteins are synthesized in ER-bound polysomes (1) attached to the ER membrane through the interaction of signal recognition particle (SRP) and membrane receptor. As soon as they enter the lumen of the organelle, they are bound to a series of molecular chaperones, including BiP, to assist correct folding (2). Upon ER stress, the accumulation of unfolded protein (UP) activates a protective signaling cascade, designated as unfolded protein response, which allows communication of ER with the nucleus via a bipartite signaling module: the bZIP28/bZIP17 and IRE1a/IRE1b-bZiP60 signaling modules. Under normal conditions, BiP is bound to bZIP28/17, keeping the transducer in an inactive configuration (4). Upon ER stress, UP causes the dissociation of BiP from bZIP28/bZIP17, which is, then, translocated to the Golgi (5), where it is proteolytically cleaved to release the bZIP28/bZIP17 domain from the membrane that, in turn, is translocated to the nucleus (6). UP accumulation also causes the oligomerization of IRE1a/IRE1b, subsequent activation of its kinase domain by phosphorylation, and the endonuclease activity (6). The activated IRE1a/IRE1b endonuclease domain promotes unconventional splicing of bZIP60 mRNA to remove a transmembrane motif-encoding fragment, generating bZIP60 spliced mRNA that is translated into a soluble bZIP60 protein (bZIP60s) (7), which otherwise would be translated into the membrane-associated bZIP60us as it occurs under normal conditions. bZIP60s is, then, translocated to the nucleus (8), where it cooperates with bZIP28/bZIP17 to upregulate UPR genes and ERAD-related genes, increasing the ER protein processing capacity under ER stress to promote recovery (9). However, if the stress persists, and ER homeostasis cannot be restored, cell death signaling pathways are activated. among them, the DCD/NRP-mediated cell death signaling is initiated with activation of AtNRP1 (10) that leads to the induction of AtNRP2 and activation of a signaling cascade that culminates with the induction of ANAC36 that binds to the VPE promoter (11) and induces the expression of VPE, the executioner of the cell death program via collapse of the vacuole. These ER stress signaling pathways are conserved in other plant species.
The detection of ER stress is mediated by membrane-associated sensors, identified both in mammals and plants. In mammals, there are three of these sensors: kinase/endoribonuclease inositol-requiring enzyme 1 (IRE1), activating transcription factor 6 (ATF6), and protein kinase RNA-like ER kinase (PERK) [15], which are regulated by the ER-resident molecular chaperone BiP (binding protein). The ER sensors initiate the UPR to restore ER homeostasis under stress condition. If the adverse physiological status is prolonged, they can initiate some alternative routes leading to cell death.
Under normal conditions, BiP is bound to the luminal domain of these receptors, keeping them inactive. With the stress progression and consequent misfolded protein accumulation, the BiP molecular chaperone function is required to prevent aggregation of the unfolded proteins. Therefore, under these stress conditions, BiP is released from the ER receptors, which leads to their activation. The three ER signal transducers act in different ways, but in convergent stress-responsive pathways. IRE1 (IRE1a and IRE1b) displays a dual biochemical activity. It harbors a ribonuclease and kinase activity at the C-terminus, responsible for the unconventional spliceosome-independent splicing of X-box binding protein 1 (XBP1) mRNA. Stress-mediated BiP release from the IRE1 N-terminus promotes IRE1 homodimerization, which sequentially activates its kinase via autophosphorylation and endoribonuclease activity, culminating on spliceosome-independent splicing of XBP1, a bZIP transcriptional factor. Under normal conditions, the XBP1u (unspliced form) is constitutively translated into a low-functional transcription factor, which is rapidly degraded by the proteasome and does not effectively activate UPR. The IRE1-mediated mRNA splicing removes an unconventional intron of 26 nucleotides, which causes a shifting frame in XBP1 mRNA translation, generating a protein of 376 amino acids instead of 261 amino acids when unprocessed. This unconventional splicing seems to prevent the degradation of XBP1s (spliced form) product by the proteasome and increase its transactivation activity, causing activation of UPR-related genes [16, 17]. Thus, the XBP1s is a soluble and functional transcription factor, which is reallocated to the cell nucleus to activate genes involved in cytoprotective pathways, such as some members of ER quality control or programmed cell death-related genes, including the apoptotic signaling kinase 1 (ASK1) and Jun-N-terminal kinase (JNK) [16, 17, 18, 19].
The ER signal transducer ATF6 is anchored to the ER membrane and harbors an N-terminal sensor domain facing the ER lumen and a C-terminal bZIP domain facing the cytosolic side. Under normal conditions, ATF6 is inactivated by BiP binding to the ER stress sensor domain. ER stress conditions promote the BiP disassociation and reallocation of ATF6 to the Golgi apparatus, where it is specifically processed by SP1 and SP2 proteolytic enzymes. The limited proteolysis of ATF6 transmembrane domain allows that the bZIP domain of ATF6 be directed to the nucleus, where it acts in concert with XBP1 to induce genes involved in ER protein processing, ER quality control, and ER-associated protein degradation (ERAD) pathway. Finally, the PERK activation upon BiP release by stress conditions promotes global translation suppression through the phosphorylation of the translation initiation factor IF2α [20]. PERK also activates the transcription factor CHOP, involved in the regulation of apoptosis-related genes [10, 21].
In plants, the UPR pathway has, at least, two arms (Figure 1). The first one activates IRE1 (IRE1a–AT2G17520 and IRE1b–AT5G24360, in Arabidopsis thaliana), and the other is transduced through bZIP membrane-associated transcription factors (bZIP17–AT2G40950 and bZIP28–AT3G10800, in Arabidopsis thaliana) [22, 23]. In the first arm of plant UPR, like in mammals, the accumulation of misfolded proteins leads to the activation of IRE1, which promotes unconventional cytosolic splicing of bZIP60 mRNA [24]. The unspliced bZIP60 mRNA, called bZIP60us, is translated into an ER membrane-associated transcription factor and does not exhibit transcriptional activity. Upon IRE1 activation by UPR, the spliced bZIP60 mRNA, called bZIP60s, does not display the transmembrane domain coding region, and its translation generates an active transcription factor, which is reallocated to the nucleus to activate UPR and cytoprotective genes, such as BiP3, CNX (calnexin), CRT (calreticulin), etc. [24, 25, 26]. This mechanism is conserved among plants, as the rice (Oryza sativa) bZIP60 orthologs, OsbZIP74 or OsbZIP50, display similar IRE-mediated mRNA splicing to render the activation of ER stress-inducible promoters [27, 28]. Likewise, in maize (Zea mays), ZmbZIP60 mRNA splicing leads to the activation of ER stress-inducible promoters [29], and, in soybean (Glycine max), the ZIP60 ortholog GmbZIP68 harbors a canonical site for IRE1 endonuclease activity and is efficiently spliced under ER stress conditions to activate UPR genes [30].
The second arm of plant UPR pathway is mediated by posttranslational modification of bZIP17 and bZIP28 transcription factors, the functional analogs of ATF6. Both bZIP17 and bZIP28 display a canonical SP1 site in their C-terminal domain, facing the ER lumen [31]. Upon stress conditions, BIP is released from the bZIP28 and bZIP17 ER sensor domain, and the transcription factors are reallocated from the ER to the Golgi apparatus, where they are processed by SP1 and SP2 proteases. These proteases remove the transmembrane domain of bZIP17 and bZIP28, exposing their cytosolic regions, which will activate UPR-related genes in the nucleus [31, 32, 33, 34]. Like the IRE1/bZIP60 signaling module of plant UPR, the bZIP28/bZIP17 arm triggers the evolutionarily conservative UPR but also accommodates cross-talk with several other adaptive signaling responses [24, 30, 31]. In summary, upon ER stress, bZIP60s and bZIP28 use a different mechanism to be translocated to the nucleus where they act in concert to induce the expression of UPR genes and ERAD-related genes to increase the ER protein processing capacity for recovery from stress.
At a physiological level, the UPR encompasses three protective mechanisms: (i) global translation suppression by PERK-mediated IF2α phosphorylation; (ii) upregulation of ER-resident molecular chaperones, and (iii) proteasome-mediated protein degradation by ERAD pathway. However, if the stress conditions are sustained and the UPR pathway fails to restore ER homeostasis, apoptotic pathways are triggered as an ultimate attempt to survive. In plants, there is a specific branch of ER stress that integrates the osmotic stress and leads to programmed cell death (PCD), the development and cell death domain-containing N-rich protein (DCD/NRP)-mediated cell death signaling (Figure 1) [12]. This cell death pathway was first identified via genome-wide and expression profiling approaches, which revealed a modest overlapping between ER and osmotic stress-induced transcriptomes of soybean seedlings treated with PEG (an osmotic stress inducer) and tunicamycin and AZC (ER stress inducers). Several genes displayed similar kinetics and a synergistic induction under combined ER and osmotic stresses, indicating that the ER stress response integrates the osmotic signal to potentiate transcription of shared target genes. Among them, two plant-specific DCD/N-rich proteins, NRP-A and NRP-B, an ubiquitin-associated protein homolog (UBA), and a NAC domain-containing protein, GmNAC81, displayed the most robust synergistic upregulation by the combination of both stresses [35]. Transient expression of NRPs or GmNAC81 in soybean protoplasts and Nicotiana benthamiana leaves demonstrated that they are critical mediators of ER stress- and osmotic stress-induced cell death in plants [36, 37, 38].
The NRP-A and NRP-B display a highly conserved DCD domain at their C-terminal protein region and a high number of asparagine residues at their more divergent N-terminus (Figure 2) [39]. Consistent with the presence of a DCD domain, overexpression of NRPs in soybean protoplasts induces caspase-3-like activity and promotes extensive DNA fragmentation. Furthermore, transient expression of NRPs in planta causes leaf yellowing, chlorophyll loss, malondialdehyde production, ethylene evolution, and induction of the senescence marker genes, which are hallmarks of leaf senescence and cell death [36, 38, 40]. The cell death response mediated by NRPs resembles a programmed cell death event. Because NRPs were the first components of the ER stress and osmotic stress-integrating cell death response to be characterized, this signaling pathway is commonly referred to as the DCD/NRP-mediated cell death response.
Schematic representation of the cell death pathway components. The predicted domains of each protein are highlighted. The indicated domains are delimited by the amino acid positions in the primary structure shown by the numbers. For ERD-15, PAM2 is a PABP-interacting motif, PAE2 is PAM2-associated element 1 motif, DEDEKERKEGKEV is a conserved sequence representing a putative motif of ssDNA-binding transcriptional regulators, and QPR is a highly conserved C-terminal QPR motif. As for GmNAC81, GmNAC30, and ANAC36, the N-terminal NAC domain is subdivided into five conserved motifs (A to E) as indicated. In the AtNRP1, AtNRP2, NRP-A, and NRP-B schemes, DCD is development and cell death domain.
Similar to NRPs, GmNAC81 (Glycine max NAC81, formerly designated as GmNAC6) is another target of the ER stress- and osmotic stress-integrating pathway that induces a senescence-like response in planta and cell death in soybean protoplasts [37, 41]. GmNAC81 belongs to the plant-specific transcriptional factor superfamily of domain-containing proteins, represented by 111 members in Arabidopsis, 151 in rice, 152 in maize, and 180 in soybean [42, 43]. Members of this family function in development and stress response. The NAC transcriptional factors display a highly conserved N-terminal domain, called NAC domain, responsible for recognition of cis-regulatory elements on target promoters and DNA binding (Figure 2). The C-terminal domain is more divergent in sequence but is undoubtedly responsible for transcriptional activity [44, 45]. In addition, a subset of NAC proteins, which also exhibits protein binding activity, harbors an additional transmembrane domain present in the membrane-tethered NAC proteins [43, 46, 47].
NRPs and GmNAC81 are induced by several different abiotic and biotic stresses in a coordinated manner, but induction of NRPs precedes the upregulation of GmNAC81. This early induction kinetics of NRPs is consistent with its capacity to activate the promoter and induce the expression of GmNAC81. These data placed GmNAC81 downstream of NRPs in the ER and osmotic stress-induced cell death pathway [37]. More recently, using reverse genetics in Arabidopsis, NRPs were confirmed to be upstream of ANAC36, the Arabidopsis ortholog of GmNAC81, in the DCD/NRP-mediated cell death signaling [40].
The early dehydration responsive (ERD) genes were first identified due to their rapid induction in response to drought stress. The ERD genes (ERD1 to ERD16) encode a set of proteins that differ in biological functions and cell localization [48]. Among them, ERD15 is a small acidic and hydrophilic protein that belongs to the PAM2 domain-containing protein family (Figure 2). The PAM2 domain is a well-characterized protein–protein interaction domain, which allows ERD15 to interact with polyA-binding proteins (PABP) regulating mRNA stability and protein translation [49]. In addition to PAM2, ERD15 contains two other domains with unknown function, designated as PAM2-associated element 1 (PAE1) and QPR.
ERD15 is a multiple stress-responsive gene that is involved in adaptation to abiotic and biotic stress. Light treatment, cold stress, and high salinity trigger ERD15 expression [50, 51]. ERD15 functions as a negative regulator of the abscisic acid (ABA)-mediated response and a positive regulator of the salicylic acid (SA)-dependent defense pathway. ERD15-overexpressing transgenic lines are less sensitive to ABA and display enhanced salicylic acid-dependent defense pathway, which was associated with increased resistance to the bacterial Erwinia carotovora of the transgenic lines [52].
Consistent with the multiple stress-responsive expression profiles, the soybean ERD15 ortholog (GmERD15) is also induced by ER and osmotic stress. GmERD15was identified using one hybrid screening that targeted the NRP-B promoter in yeast. As an upstream member of the NRP-mediated cell death response, GmERD15 binds the NRP-B promoter region in vivo and in vitro and induces the NRP-B expression [53]. Despite its role as a transcription factor, GmERD15 does not harbor a typical DNA-binding motif, but instead, it contains a conserved sequence of 13 amino acids at positions 71–83 (DEDEKERKEgKEv), which is a part of a tripartite motif domain derived from ssDNA-binding transcriptional regulators [54]. Accordingly, the GmERD15 binding site was mapped to a 12-bp palindromic sequence −511AGCAnnnnnTGCT−500 on the NRP-B promotor in both single-stranded and double-stranded configurations [53].
As components of the DCD/NPR-mediated cell death signaling, NRPs and GmNAC81 are critical mediators of cell death derived from ER stress and osmotic stress signals. More recent progress toward deciphering this branch of stress-induced cell death signaling includes the identification of two additional downstream components, the NAC transcriptional factor (GmNAC30) and the vacuolar processing enzyme (VPE) [55].
GmNAC30 was identified as a nuclear partner of GmNAC81 via two-hybrid screening using GmNAC81 as a bait. GmNAC30 and GmNAC81 exhibit similar expression profiles and cell death activity. They are upregulated by ER stress, osmotic stress, and by the cell death-inducer cycloheximide. Consistently, GmNAC30 promotes cell death when transiently expressed in soybean protoplasts and, as a downstream component of the cell death signaling, is induced by expression of NRP-A and NRP-B.
GmNAC30 interacts with GmNAC81 in vitro and in vivo, the complex formed binds to common cis-regulatory sequences in target promoters and synergistically regulates hydrolytic enzyme promoters, including the caspase-1-like vacuolar processing enzyme (VPE) gene, which is involved in PCD in plants [55]. Consistent with their transcriptional function as a heterodimer, GmNAC81 and GmNAC30 display overlapping and coordinate expression profiles in response to multiple environmental and developmental stimuli. Therefore, the stress-induced GmNAC30 cooperates with GmNAC81 to activate PCD through the upregulation of the cell death executioner VPE.
VPE is a vacuole-localized cysteine protease that exhibits caspase-1-like activity and hydrolyzes a peptide bond at the C-terminal side of aspartate and asparagine residues [56]. It is synthesized as an inactive preprotein precursor, which is self-catalytically converted into the active mature form, under a processing step that resembles the activation of caspase 1 (Figure 2). It has been associated with Tobacco mosaic virus-induced hypersensitive cell death and developmental PCD [57, 58]. As an executioner of a cell death program, VPE is self-activated by hydrolytic cleavage and, in turn, mediates the initial activation of vacuolar enzymes, which degrade the vacuolar membrane and initiate the proteolytic cascade leading to PCD. Therefore, VPE activation may result in vacuolar collapse-mediated cell death, a type of plant-specific programmed cell death.
The discovery of VPE as a downstream target of the coordinate action of GmNAC81 and GmNAC30 underlies a mechanism for the execution of the ER and osmotic stress-induced cell death program (Figure 1). This model holds that prolonged ER and osmotic stresses induce the expression of the transcriptional activator GmERD15 to target the NRP promoter. The upregulation of NRPs initiates a transduction signaling that leads to the induction of GmNAC81 and GmNAC30, which cooperate to activate the VPE promoter and expression. Activation of VPE promotes the disintegration of vacuoles, initiating the proteolytic cascade in plant PCD. As vacuole-triggered PCD is unique to plants, the regulatory circuit linking the stress signal to activation of VPE is fundamentally composed of plant-specific signaling components.
The DCD/NRP-mediated programmed cell death pathway is conserved and operates with similar regulatory mechanisms in plants [40]. Soybean prototypes of each component of the cell death pathway were used to search for orthologs in the Arabidopsis genome (Figure 3) [30]. Arabidopsis AtNRP1 is most closely related to GmNRP-A and GmNRP-B, whereas a third homolog GmNRP-C was related to AtNRP-2. GmNAC81 and its paralog share sequence conservation with the Arabidopsis ortholog ANAC36 (At2G17040), whereas the predicted Arabidopsis ortholog of soybean VPE was identified as At4G32940/γVPE. Transient expression of the selected Arabidopsis orthologs of pathway components (AtNRP-1, AtNRP-2, ANAC36, and γVPE) induces cell death in Nicotiana benthamiana leaves with the appearance of hallmarks of PCD and leaf senescence, including DNA fragmentation, leaf yellowing, chlorophyll loss, and lipid peroxidation [38]. In addition, knockout lines for each one of pathway genes in Arabidopsis display enhanced tolerance to ER stress-mediated cell death induction. Very importantly, the stress induction of AtNRP2, ANAC36, and γVPE was dependent on the AtNRP1 function, confirming the upstream position of AtNRP1 in the cell death pathway. Therefore, in Arabidopsis, the execution of the cell death program has been proposed to occur through AtNRP1-mediated induction of the AtNRP2-ANAC36-γVPE signaling module. Nevertheless, functional information about the GmERD15 and GmNAC30 orthologs in Arabidopsis is lacking, and these pathway components have not been identified yet in Arabidopsis. Both in soybean and Arabidopsis, the DCD/NRP-mediated cell death pathway is modulated by the ER-resident molecular chaperone BiP, which negatively regulates the gene expression and activity of these cell death-inducing genes [13, 40].
Integration of developmental signal and stress signals into the DCD/NRP-mediated cell death response. Leaf senescence, ER stress, and osmotic stress induce the expression of ERD15-regulated NRP-A that in turn upregulates NRP-B to initiate a signaling cascade that culminates with the induction of GmNAC30 and GmNAC81 expression. The NAC transcription factors form a heterodimer to fully induce the activation of VPE promoter, which leads to VPE upregulation and subsequent execution of a cell death program. The ER-resident molecular chaperone BiP acts as a negative regulator of cell death by modulating the expression and activity of the cell death pathway components. The DCD/NRP-mediated cell death signaling is conserved in other plant species, and the Arabidopsis orthologs are shown on the right.
Plants can negatively modulate the NRP/DCD-mediated cell death response to suit the cellular balance during the stress conditions. Moreover, this modulation improves the cellular stableness and consequently increases the plant tolerance to stress conditions in an essential process that is required for plant acclimatization and development. The molecular chaperone BiP plays a crucial role as a negative regulator of NRP/DCD-mediated cell death response. BiP belongs to the HSP70 family, which is essential to protect the cells against environmental stresses and to restore the cell homeostasis [59].
The molecular chaperone BiP has a catalytic site at the amino-terminal region and a substrate-binding site at the carboxy-terminal region [60]. BiP is involved in the regulation of several processes in the endoplasmic reticulum, a critical organelle that is related to responses to abiotic and biotic stress in plants. In the ER, BiP acts as a sensor that responds to quantitative and qualitative changes in the ER by regulating the activity of ER stress transducers [61]. Furthermore, BiP coordinately regulates the cell death signaling, which connects the signals from osmotic and ER stress in a DCD/NRP-dependent manner [35, 36, 38].
BiP attenuates the NRP/DCD-mediated cell death signal propagation by the modulation of expression and activity of the pathway signaling components (Figure 3). BiP overexpression in soybean attenuates ER stress- and osmotic stress-mediated cell death, a phenotype that is linked to a delay in the induction of GmNRP-A, GmNRP-B, and GmNAC81 under ER stress and osmotic stress [38]. Furthermore, enhanced accumulation of BiP in tobacco (Nicotiana tabacum) prevents the GmNRP- and GmNAC81-mediated induction of cell death-associated physiological and molecular markers, whereas silencing of endogenous BiP enhances the cell death response.
In addition to alleviating ER and osmotic stress-mediated cell death, the BiP overexpression in plants has also been shown to increase their tolerance to water deficits [62, 63, 64]. Enhanced accumulation of BiP in soybean, tobacco, and Arabidopsis promotes a delay in drought-induced senescence and wilting of leaves leading to a higher survival rate of overexpressing lines under water-deficit regimes [12, 38, 40, 63, 64]. The BiP-mediated tolerance mechanism is not associated with conventional mechanisms of drought tolerance and avoidance, as the BiP-overexpressing lines do not display lower photosynthesis and transpiration rates than untransformed lines under drought, and the stomata closure and root growth are not stimulated under water deprivation. Furthermore, the BiP-overexpressing lines exhibit a lower induction of drought-related genes than WT under water-deficit conditions, and the abscisic acid content in BiP-overexpressing plants is similar to untransformed lines, indicating that the BiP-mediated drought tolerance mechanism is independent on ABA [59, 64, 65]. Under drought conditions, the only variations observed in BiP-overexpressing lines are a delay in drought-induced leaf senescence and an attenuation in the drought induction of PCD-associated marker genes, which is associated with the protective function of BiP as a negative modulator of the DCD/NRP-mediated cell death response. A metabolomic approach was used to detect the metabolite profile of BiP-overexpressing lines under drought conditions [65]. Due to a higher osmolyte accumulation, mainly amino acids, the BiP-overexpressing plants can maintain the leaf turgidity upon drought stress, which is a phenotypic hallmark of the BiP-mediated tolerance to drought. The BiP-overexpressing lines also display a higher accumulation of salicylic acid and upregulation of SA-responsive genes, which is associated with accelerated hypersensitive response triggered by Pseudomonas syringae pv tomato in soybean and tobacco [59, 65]. The SA signaling also activates the antioxidative metabolism, which may be linked to the BiP protective function to drought. Very importantly, the BiP modulation of the DCD/NRP-mediated cell death response does not impair the plant growth and development.
Leaf senescence is a natural process in plant development, which begins with a physiological transition between active photosynthetic leaves to degenerative and nutrient-recycling leaves. The classical age senescence-related symptom is the leaf yellowing caused by generalized chlorophyll loss. The age-induced senescence or naturally programmed leaf senescence, hereafter referred to as leaf senescence, occurs by plant aging and is precisely regulated by senescence-associated genes (SAGs) [66, 67].
Many SAGs are environmental- and stress-responsive genes, integrating a convergent regulatory cascade between natural plant development and stress-induced PCD [68]. At the molecular level, the onset of senescence is accompanied by a massive reprogramming of gene expression, probably controlled by senescence-associated transcription factors. Among these, several NAC transcription factors have been associated with senescence regulation based on high-resolution temporal expression profiles [69].
In soybean, a transcriptomic analysis of senescing leaves reveals that 44% of the GmNAC genes were differentially expressed at the onset of leaf senescence. The most representative subfamilies of soybean senescence-associated NAC genes were the abiotic stress-induced SNAC-A (ATAF) subfamily, in which 90% of the members were differentially expressed during senescence, followed by the biotic stress-induced TERN subfamily, displaying 80% of the members differentially expressed during leaf senescence [43]. GmNAC30 and GmNAC81, which belong to the SNAC-A and TERN subfamilies, respectively, are among the upregulated genes by leaf senescence [43, 59]. These results raise the hypotheses that the (i) DCD-NRP/NAC/VPE signaling module may integrate stress-induced with natural leaf senescence and (ii) other NAC genes may be involved in integrated circuits between age- and stress-induced cell death pathways.
Regarding the first hypothesis, several lines of evidence indicate that the regulatory circuit NRPs/GmNAC81:GmNAC30/VPE integrates osmotic stress- and ER stress-induced PCD response with natural leaf senescence. First, not only GmNAC30 and GmNAC81 but also the other cell death pathway components, NRP-A, NRP-B, and VPE, are induced by leaf senescence [43, 59, 70]. Second, the activity of VPE is also induced during the onset of leaf senescence [59]. Third, transient expression of the soybean components of ER stress- and osmotic stress-induced cell death response, NRP-A, NRP-B, GmNAC81, and GmNAC30, as well as the Arabidopsis orthologs AtNRP1, AtNRP2, ANAC36, and γVPE, in protoplasts and in planta induce a cell death response bearing the hallmarks of leaf senescence and PCD. These symptoms include the induction of caspase 1-like activity and DNA fragmentation, chlorophyll loss, protein degradation, enhanced lipid peroxidation, and the induction of senescence-associated marker genes [36, 37, 38, 40, 55]. Fourth, enhanced accumulation of BiP, which negatively regulates the NRPs/GmNAC81:GmNAC30/VPE signaling module, also promotes a delay in leaf senescence in transgenic plants [59]. Finally, GmNAC81 is a positive regulator of naturally programmed leaf senescence [70]. Although leaf senescence is genetically programmed in an age-dependent manner, it can be triggered by environmental cues and is also positively and negatively regulated by various plant hormones. GmNAC81 and GmNAC30 are induced by the phytohormones ABA, jasmonic acid (JA) and salicylic acid (SA), which are positive regulators of senescence, and GmNAC81-overexpressing lines display high levels of ABA, mimicking the enhanced endogenous levels of this hormone during leaf senescence [70, 71]. Consistent with a role in leaf senescence, the overexpression of GmNAC81 in soybean plants accelerates leaf senescence, a phenotype associated with extensive leaf yellowing, increased chlorophyll loss, faster photosynthetic decay, and enhanced expression and activity of the GmNAC81 direct target VPE, than untransformed, wild-type plants. Conversely, suppressing GmNAC81 expression delays leaf senescence and decreases the expression of GmNAC81 direct target genes, including VPE [70]. Therefore, GmNAC81 is involved in developmentally programmed leaf senescence. Furthermore, ER stress- and osmotic stress-induced PCD is integrated with natural leaf senescence through the NRPs/NACs/VPE regulatory circuit.
Since the discovery of the ER stress- and osmotic stress-induced DCD/NRP-mediated cell death response, considerable progress has been achieved toward deciphering the components and regulation of the pathway (Figure 3). We now know that the combination of multiple stresses synergistically activates a plant-specific PCD response that is initiated by induction of the stress-responsive transcription factor GmERD15, which, in turn, binds and activates the DCD/NRP promoter. Induction of the DCD/NRP genes NRP-A and NRP-B leads to the activation of a signal cascade that culminates with the upregulation of the transcription factors GmNAC81 and GmNAC30. The NAC transcription factors form a heterodimer to activate the expression of hydrolytic enzymes, including VPE, an executioner of vacuole-triggered programmed cell death. The stress-induced DCD/NRP-mediated cell death response is conserved in plants with similar regulatory mechanisms and represents a shared response to multiple stress signals. As a negative regulator of the stress-induced DCD/NRP-mediated cell death response, overexpression of the ER-resident molecular chaperone BiP delays drought-induced senescence in tobacco and soybean plants and confers the increased adaptation of these transgenic lines under water deprivation conditions. This DCD/NNP-mediated stress-induced cell death program is also activated during age-dependent leaf senescence and contributes positively for the progression of the developmentally programmed senescence. Therefore, the plant-specific NRPs/NACs/VPE signaling module represents a regulatory circuit integrating stress-induced with natural leaf senescence.
We thank the Brazilian government agencies, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for financial support.
The authors declare no conflict of interest.
Supporting women in scientific research and encouraging more women to pursue careers in STEM fields has been an issue on the global agenda for many years. But there is still much to be done. And IntechOpen wants to help.
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