Morpho-physiological indicators of the well-watered and moderately drought-stressed cotton genotypes.
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\r\n\tIn this book Advanced application of radionuclides are introduced. New global trends on safe application of radionuclides in human life is elucidated.
Drought is an important environmental stress exerting a critical effect on plants that can reduce their productivity, on average, up to 50% [1]. Approximately one third of Earth’s arable land all over the world suffers from chronic water deficiency for agriculture and by various estimations; in 2050s, this area can be doubled [2]. Particularly, in Central Asia, located mostly in desert zones, the first-limiting factor of crop yield is water deficit and the agriculture can be practiced only with additional irrigation. However, the irrational use of water resources of the region for cotton production in the past has lead to an excessive soil salinization and to the exhaustion of its largest water resource—the Aral Sea. Therefore, revealing the adaptation potential of local agricultural crops to water deficit and creating their drought-tolerant genotypes are an important task: this would allow, in particular, to obtain higher cotton yield and quality in conditions of limited water resources and to improve local environment by stopping desertification of the region.
\nCreating drought-tolerant genotypes of agricultural crops is complicated because the lack of systematic knowledge on physiological parameters reflecting the genetic potential for improved productivity under conditions of water deficiency. The effect of drought stress on the photosynthetic performance and drought-induced morpho-physiological, biochemical and biophysical changes in various plant species have been extensively studied; stomatal and non-stomatal limitations to photosynthesis, their role and possible mechanisms have been suggested [3]. These studies have shown that photosynthetic performance is very informative and sensitive indicator of stress effects of drought in plants.
\nNowadays, the methods of chlorophyll fluorescence control along with the classical measurements of photosynthesis based on gas-exchange analysis are widely used by agronomists in monitoring of crops and their response to environmental stresses [4]. Revealing physical characteristics of chlorophyll fluorescence in plant leaves and employing achievements in laser physics, optoelectronics and computer technologies allowed developing a variety of efficient experimental methods and easy to use devices for measuring such key fluorescence parameters, as a maximal (saturated) and a minimal (dark) fluorescence, a prompt and a delayed fluorescence, a kinetics of induction of chlorophyll fluorescence and their relationship with quantitative indicators of photosynthesis in plants [5, 6]. These methods are fast, noninvasive and estimate the photosynthetic performance of plants even under mid-day solar radiation, and portable devices commercially manufactured on their basis determine the parameters of plant photosynthetic performance with multiple replication of measurements and recording the results in a memory for subsequent statistical processing using relevant computer programs [7, 8].
\nHere, the results of long-term effect’s study of drought on the chlorophyll fluorescence and morpho-physiological indicators of cotton plants grown under field conditions are described. Literature on researches concerning to mechanisms of stress effect of drought on photosynthesis in plants are analyzed. The long-term effect of drought on cotton plants has been studied during the key period of their ontogenesis — in flowering and maturing stages from last July to last September by simultaneously measuring indicated parameters in well-watered and moderately drought-stressed plants. Correlations between the chlorophyll fluorescence and morpho-physiological indicators (leaf blade area and thickness, relative water content and transpiration) have been defined in three genotypes of cotton with different degrees of drought tolerance.
\nComparative measurements of the operating quantum efficiency of photochemistry in Photosystem II, ФPSII, and its changes during the day time in well-watered and moderately drought-stressed plants have shown that in contrary to the widely accepted idea on tight links between ФPSII and the quantum efficiency of CO2 uptake [9], and decline of photosynthesis in plants under drought stress [10, 11], the sustainable higher values of ФPSII in drought-stressed plants have been registered [12, 13]. It was also defined considerable changes in morpho-physiological parameters under drought stress.
\nFor better understanding of mechanisms of such an unexpected increase in the quantum efficiency of primary photochemistry, the chlorophyll fluorescence was measured simultaneously with the gas-exchange analysis at different light intensities and CO2 concentrations [14]. Drought-stressed plants displayed elevated rates of photorespiration playing a protective role in conditions of water deficit, when plants can gradually adapt to such a stress, regulating various phases of photosynthetic reactions.
\nThe measurement of photoacoustic waves generated in plant leaves on application of a modulated light simultaneously with the chlorophyll fluorescence allowed us to determine quantitatively the magnitude of photosynthetic oxygen evolution. This has an especial importance in the case of elevated photorespiration, when tight links between ФPSII and the quantum efficiency of the CO2 uptake is broken. Photobaric component of the photoacoustic waves at low-modulation frequencies (~10 Hz) originated in the photosynthetic oxygen evolution process [15, 16], as quantitative indicator of the photosynthetic performance of plants, may be used for the calibration of the values ФPSII determined in chlorophyll fluorescence measurements.
\nIn this way, the chlorophyll fluorescence parameters measured simultaneously with morpho-physiological indicators of plants proposed for monitoring of the drought tolerance of various cotton genotypes in the field that can be applied in the practice of a plant breeding.
\nThree local genotypes of cotton (Gossypium hirsutum L.), Navbakhor, Liniya-49, and Gulsara were grown on the two levels of irrigation: under well-watered and moderately drought-stressed conditions [17] at the experimental cotton station of the Institute of Genetics and Plant Experimental Biology, Uzbekistan Academy of Sciences, Tashkent (41°10´N, 69°07´E, 400 m above sea level), in 2013–2014. All plants were sown on 10th April with the scheme of 90 cm (distance between rows) × 20 cm (distance between plants) × 1 (amount of plants per hole). Thousand plants of each genotype and water treatment were grown in 4 rows, 250 plants each. During the entire period of ontogenesis, well-watered plants were irrigated 5 times: 1–before flowering, 3–during flowering-maturing, and 1–in maturing stages, and the drought-stressed plants–3 times: in the scheme 1—2—0. Thus, moderate drought stress was induced in the most sensitive stage of cotton plants—in mass flowering-maturing period. During this period, rainfall did not occur. All other growth conditions, including content of nutrients in soil, were the same.
\nThe chlorophyll fluorescence was measured in attached leaves by using portable chlorophyll fluorometer Mini-PAM (Walz, Effeltrich, Germany) allowing up to 3000 measurements in the field without battery recharging [7]. The Mini-PAM fluorometer measures the chlorophyll fluorescence parameters even under mid-day solar radiation by means of simultaneous application of a CW measuring light and saturating light flashes. Measurements were carried out in the early morning, from 7.00 to 8.00, on the third, matured leaves with 10-fold replication. In most of the experiments, the operating quantum efficiency of primary photochemistry,
The gas-exchange measurements were carried out using photosynthesis analyzer LI-6400 (Licor, USA) at temperature 24°C [21]. The curves of CO2 response were measured in leaves of both water treatments by means of gradual lowering of the external CO2 concentration, from 400 μmol mol-1 to 0 μmol mol-1 at PPFD 1000 μmol m-2 s-1, and the light response curves—at ambient СО2 concentration with step-by-step increasing of PPFD from 0 μmol m-2 s-1 to 2000 μmol m-2 s-1. The light and CO2 responses of the chlorophyll fluorescence and the photosynthesis were measured after adaptation of leaves to each value of PPFD and CO2 concentration during 15 min. The operating values of the minimum fluorescence under continuous illumination during the measurements, F′0, were calculated according to [22] using the equation
Relative water content and transpiration of plant leaves were determined by their weighting [23]. In addition, a leaf thickness and a leaf blade area were also measured in each cotton genotype. For estimation of the magnitude and diurnal variations of photoinhibition, the values of ФPSII have been consistently measured simultaneously in both well-watered and drought-stressed plants every hour during 24 h.
\nPhotoacoustic spectrometer of special design with ~1 cm3 sample chamber having higher sensitivity at low (10–250 Hz) frequencies of light modulation [24] has been used for measuring photoacoustic characteristics of plant leaves. The sources of a CW measuring light and saturating light flashes of the spectrometer were a semiconductor LED (650 nm, 20 mW) and a halogen lamp (400–700 nm, 20 W) with a mechanical chopper, respectively. Intensity of the measuring light was supported as 50–100 μmol m-2 s-1 and intensity of the saturating flashes did not exceed 2500 μmol m-2 s-1. The photobaric component was selected from the total photoacoustic waves generated in a plant leaf at application of low-frequency (10 Hz)-modulated light by recording quadrature signal from a lock-in amplifier [25].
\nDrought stress is primarily affected to photosynthetic performance of plants. The long-term drought effect is expressed as reducing/delaying of a plant growth and development, premature leaf senescence, and related reduction in a crop productivity [26, 27]. The dispute, what, mainly, limits photosynthesis under conditions of water deficiency: stomata closure or impairment of the metabolism is long enough [28, 29], but in the past decade, closure of stomata was perceived by experts as the predominant factor in mild and moderate drought stress [30].
\nThe first response of a plant to onset of drought stress is the stomata closure and associated reduction of the relative water content of leaves and intracellular CO2 concentration, Ci [3, 31]. This, in turn, causes decrease in a leaf turgor and a water potential [32]. In such a condition, gas-exchange analysis in plant leaves would be an informative technique for assessment of stomatal limitation to CO2 assimilation.
\nNon-stomatal mechanisms of the photosynthesis limitation under long-term or severe drought in the soil include changes in chlorophyll synthesis [33], structural changes in photosynthetic apparatus and depressing the Calvin cycle enzymes activities, which reduces crop yield [34] and decline in Rubisco activity [35, 36].
\nShort-term or mild drought-induced non-stomatal limitations to photosynthesis have smaller magnitude than stomatal ones. Closure of stomata and limited access of CO2 bring about reduced utilization of the energy of electron transport, and, accordingly, over-excitation of the plant photosynthetic apparatus. This, accordingly, increases the susceptibility of the system to photo-damage. Accumulation of singlet oxygen or superoxide radicals, when a dynamic balance between producing of such reactive substances and functioning of the plant antioxidant defense system is broken, may cause destruction of photosynthetic proteins and membrane lipids [37, 38].
\nReduced rate of transpiration, especially at higher ambient temperatures, increases the heat accumulation and relevant increase in leaf temperature. The latter can also cause decline of the plant photosynthetic performance under drought [30].
\nA number of experiments have shown that the closure of stomata is controlled, mostly, by reducing soil water content, but not leaf water status. This suggests response of stomata to a chemical signal from roots, i.e. presence of abscisic acid produced by dehydrating roots, while a leaf water status is constant [39, 40]. The same time it means that the efficient way to control the stomatal conductance is to change the soil water content even preserving constant level of leaf water status.
\nActivity of the photosynthetic electron transport chain is rigidly regulated by the availability of CO2 in the chloroplast, limited by closure of stomata under drought stress [41]. Leaf dehydration leads to shrinking of cells and accordingly reducing of their volume. This causes an increase in the internal viscosity of the cell contents, and interaction between proteins and, consequently, their aggregation and denaturation [42].
\nComparison of the results from different studies is quite difficult due to the essential variations in responses of the stomatal conductance and photosynthesis to changes of leaf water potential and relative water content in different genotypes [3]. It is considered as well established that drought-induced stomata closure declines the net photosynthesis in all plant species, though, with different magnitudes. That is why comparative studies of the photosynthetic parameters in different plant genotypes under drought stress may provide an important information concerning to the photosynthetic performance and adaptation potential of plants to moderate long-term drought.
\nAnalysis of the chlorophyll fluorescence and photosynthesis in plant leaves has revealed that in conditions favorable for photosynthesis, i.e. lack of environment stresses, at low light intensities, etc. when alternative mechanisms of light energy utilization did not required, the quantum efficiency of photochemistry is tightly linked with quantum efficiency of CO2 fixation [9], and the photosynthesis rate is not sensitive to mild under drought stress [10, 43]. In this condition, photorespiration increases and its magnitude depends on the light intensity [44]. In a number of researches, the reduction in ФPSII has been observed under long-term drought, which has been attributed, mostly, to reducing of photochemistry and, in less extent, to dissipative processes in the plant photosynthetic apparatus. However, in some other researches, the increasing ФPSII has been observed in plants exposed to moderate long-term drought [12, 13]. Such contradiction in behavior of ФPSII may be explained by a heterogeneity of the photosynthetic performance across the leaf blade [14, 45]. Thus, simultaneous analysis of chlorophyll fluorescence and photosynthesis in plant leaves may reveal mechanisms and magnitude of protective changes in plants under drought stress, and correlations between changes in chlorophyll fluorescence parameters and morpho-physiological indicators, traditionally used for estimation of drought tolerance of plants, may be used as an effective instrument for monitoring of plants in the field.
\nThe operating quantum efficiency of photochemistry, ФPSII, has been determined simultaneously in well-watered and moderately drought-stressed plants of three genotypes of cotton cultivated in Uzbekistan with the aim of estimating the magnitude of the effect of drought on the photosynthetic performance and monitoring its changes during a key period of the ontogenesis—in flowering and maturing stages from last July to last September [12, 46]. Figure 1 shows the results of this experiment. The dates of measurements are shown on the X-axis. Stressed plants of all cotton genotypes display higher values of ФPSII in comparison with well-watered plants. Moreover, in the drought-tolerant plants of Navbakhor, this increase was maximal (up to 15% over the most period of measurements), while in Gulsara characterized by lower drought tolerance, it was minimal (approximately 2%). And, in Liniya-49 having an intermediate degree of drought tolerance had intermediate values for differences in ФPSII. Irrigation of the drought-stressed plants on 10th September shortened this difference, though, with different extent in different genotypes.
\nThe changes in ФPSII in leaves of three genotypes of cotton: Navbakhor (a), Liniya-49—(b) and Gulsara—(c) growing in well-watered (•) and moderately drought-stressed (○) conditions during a long period of their ontogenesis.
Measurements of morpho-physiological indicators in plants of all genotypes have demonstrated considerable reduction in leaf relative water content and of leaf blade expansion and increase in leaf thickness under long-term drought stress. These changes are presented in Table 1. It is seen that in the most drought-tolerant cotton genotype Navbakhor, these changes are maximal, and in Gulsara having lower drought tolerance, these are minimal. Correlations between ФPSII and these morpho-physiological indicators have been defined in all three genotypes, but with different extent. The last may be attributed to the possibility of other protective reactions in plants affected to long-term drought stress [47].
\nMorpho-physiological indicators | \nWater treatment | \nCotton genotypes \n | \n||
---|---|---|---|---|
Navbahor | \nLiniya-49 | \nGulsara | \n||
Relative water content, % | \nWell-watered | \n79.4 | \n78.8 | \n77.4 | \n
Drought-stressed | \n72.5 | \n74.4 | \n74.3 | \n|
Percentage of the difference | \n8.7% | \n5.6% | \n5.0% | \n|
Leaf blade area, m2\n | \nWell-watered | \n71.1 | \n77.7 | \n80.9 | \n
Drought-stressed | \n63.1 | \n73.0 | \n77.1 | \n|
Percentage of the difference | \n11.3% | \n6.1% | \n4.7% | \n|
Relative leaf thickness, g m-2\n | \nWell-watered | \n0.853 | \n0.974 | \n0.987 | \n
Drought-stressed | \n0.981 | \n1.09 | \n1.052 | \n|
Percentage of the difference | \n15.0% | \n11.9% | \n6.6% | \n
Morpho-physiological indicators of the well-watered and moderately drought-stressed cotton genotypes.
Leaf transpiration was lower in drought-stressed plants than in well-watered plants of all genotypes for 5–15% (not shown), which may be considered as typical for the field-grown cotton plants [48]. However, diurnal changes in transpiration of plants were much more than differences between two treatments, therefore reliable correlations between changes in the transpiration and the chlorophyll fluorescence parameters under drought stress were not established.
\nDiurnal changes in ФPSII measured in leaves of the cotton genotype Navbakhor grown in well-watered (•) and moderately drought-stressed (○) conditions in the field.
For determination of changes in the photosynthetic performance of plants under drought stress and kinetics of photoinhibition over the day, the quantum efficiency of photochemistry has been measured hourly during 24 h. Figure 2 shows such dependencies measured in well-watered and drought-stressed plants of Navbakhor. As shown in previous figure, in the drought-stressed plants, ФPSII is higher than in well-watered plants during all the day, including a night time. In addition, decline of ФPSII in mid-day in the drought-stressed plant is smaller but occurs for longer time [12]. Such a photoinhibitory depression of the primary photochemistry under high-intensity solar radiation is characterized by various components with different relaxation periods [49, 50]. Obviously, adaptive changes in the structure and functioning of the plant photosynthetic apparatus under moderate long-term drought may bring about depressing, mainly short-period, components of photoinhibition and its long-period components will dominate in drought-stressed plants [51]. Such changes in the proportion of different components of photoinhibition results in decreasing of the amplitude and reshaping of the form of diurnal changes ФPSII as it is shown in Figure 2. It should be noted that difference in values of ФPSII measured in well-watered (0.34) and drought-stressed (0.48) plants at mid-day, 0.14, is considerably higher than those in other periods of the day. This fact may be considered as enhancing of photorespiration that may contribute in ФPSII only as a prompt component.
\nTherefore, protective response of cotton plants to drought stress expressed in photosynthetic indicators is the increase in quantum efficiency of primary photochemistry, in morphology is the increase of leaf thickness with decreasing leaf blade expansion and in physiology is the reduce in transpiration. If reduce in the leaf blade expansion and transpiration may be explained logically by considerations of minimizing the moisture loss [47], increase of ФPSII looks as somehow contradictory with the literature data: at the onset of drought stress, the plant should response by reducing photosynthesis to protect the photosynthetic apparatus [52]. At constant values of efficiency of alternative ways of energy utilization, this has to bring about lower quantum efficiency of photochemistry. Then, the excessive energy of absorbed light may be utilized by enhancing the activity of an alternative channel—photorespiration. Lastly, in C3 plants could be significant, particularly in cotton, which typical growth conditions are associated with higher temperatures and water deficiency. At present, protective role of photorespiration under environmental stresses are poorly studied and published researches on this matter is very minor [53].
\nThus, cotton genotypes with different degrees of drought-tolerance studied displayed specific changes in the chlorophyll fluorescence parameters, as well as in morpho-physiological indicators under long-term drought stress. Diurnal curves of ФPSII variations in well-watered and moderately drought-stressed plants provide information on the magnitude and different time components of photoinhibition developed under high-intensity solar radiation.
\nPhotoacoustic waves generated in plant leaves at application of modulated light have been studied for precise control of the photosynthetic performance and quantitative estimation of the photosynthetic oxygen evolution. Photobaric component of the photoacoustic waves related to photosynthetic evolution of oxygen has been measured in the photoacoustic cell of special design with a small measuring chamber (~1 cm3) in lock-in amplifier by selecting quadrature signal at low frequencies [15, 54]. Figure 3 shows kinetics of changes of the photoacoustic signal from the well-watered (relative water content 100%) and short-term dehydrated (relative water content 65%) leaves of the cotton genotype Navbakhor, generated at application of low frequency (10 Hz) measuring light. It is shown from the figure that the steady-state photoacoustic signal considerably declines at application of additional CW light of high intensity (~2500 μmol m-2 s-1) to plant leaf, which saturates photosynthetic oxygen evolution process and, accordingly, excludes periodic changes of pressure in the measuring chamber, which is the photobaric wave. Therefore, relative change in the photoacoustic signal (ratio of amplitude of change to the total photoacoustic signal) may be used as a measure of the photosynthetic oxygen evolution. In experiments, before measuring photoacoustic signals, the plant leaves were adapted to dark for 10 min. After reaching the steady-state photoacoustic signal, the saturating CW light was applied, which causes decrease in the photoacoustic signal for 0.82 (Figure 3a) in the well-watered leaf and for 0.50 (Figure 3b) in the dehydrated leaf. Thus, the photoacoustic measurements have shown that photosynthetic oxygen evolution in plant leaves depresses in short time water deficiency: decrease in the relative water content for 45% causes decrease of photosynthetic activity 1.5 times. Simultaneous measurements of ФPSII in these two samples displayed decline of the operative quantum efficiencies of photochemistry in the same ratio (0.75:0.51). However, the advantage of photoacoustic measurements is evident in the case of significant level of photorespiration in plant leaves, when direct correlation between ФPSII and the net photosynthesis is disturbed (see the next section).
\nInduction curves of the photoacoustic signal generated in leaves of the cotton genotype Navbakhor with relative water content 100% (a) and 65% (b). Arrows up and down show switching on and off, respectively, the measuring (dashed arrows) and saturating (bolt arrows) lights.
Electron transport rate (ETR) and photosynthesis in cotton plants of both water treatments have been measured simultaneously for revealing the role and magnitude of alternative channels for utilization of the energy of electron transport and obtaining new insights into mechanisms of adaptation of the plant photosynthetic apparatus to long-term drought stress. Indicated photosynthesis parameters have been determined at CO2 concentrations 0–400 μmol mol-1 under constant PPFD of 1000 μmol m-2 s-1 and under PPFD of 0–2000 μmol m-2 s-1 at ambient CO2 concentration in plants of genotype Navbakhor (Figure 4). It is seen that the rate of CO2 assimilation (AG) increases linearly with increase of intracellular CO2 concentration, Ci, while the dependence ETR versus Ci is non-monotonic: sharp increase of ETR with increase of CO2 concentration at Ci < 100 μmol mol-1, further saturates on the level of ETR ~200 μmol m-2 s-1. The measurements were carried out in the field, early morning, from 7.00 to 8.00 at temperature 22–24°C.
\nResponse of the photosynthesis, AG, electron transport rate, ETR, and photorespiration, estimated as ETR/4-AG, to CO2 concentration in leaves of the cotton genotype Navbakhor grown in well-watered (closed symbols) and moderately drought-stressed (open symbols) conditions in the field.
At higher light intensities and/or low CO2 concentrations, the plant photosynthetic apparatus cannot cope with the coming light energy and a portion of this energy has to be utilized through alternative channels; photorespiration or some other processes, including Mehler reaction, may play a role of a sink for electrons transported through the photosynthetic electron transport chain [55]. In most of the cases, excluding severe drought stress, the photorespiration considered as prevailing mechanism of utilization of such an excessive light energy [56]. The magnitude of this energy utilization may be estimated by comparing ETR and photosynthesis. Assuming that assimilation of one molecule CO2 requires four electrons transported through the chain, the amount of photorespiration may be defined by dividing ETR by four and subtracting the photosynthesis [55]. By calculating this way, values of the photorespiration rate are also presented in Figure 4: photorespiration increases sharply at low concentrations up to 100 μmol mol-1, and further slowly drops with increase of CO2 concentration. The fact seems reasonable, because CO2 is a product of photorespiration. Figure 4 shows that drought stress noticeably increases ETR and slightly decreases the photosynthesis in cotton plant leaves. As a result, the photorespiration in drought-stressed leaves calculated as above is considerably higher than in well-watered plants, especially at higher CO2 concentrations. In addition, the effect of drought stress to “dark” respiration has been measured in plants of both water treatments simultaneously with the quantum efficiency of primary photochemistry (Table 2). The “dark” respiration, as an additional source of bioenergy necessary for supporting vital biochemical reactions in plants, was considerably higher in drought-stressed plants. The same occurred with the quantum efficiency of photochemistry, but with less magnitude.
\nWater treatment | \nRD\n | \nФPSII\n | \n
---|---|---|
Drought-stressed | \n3.8 ± 0.5 | \n0.67 ± 0.023 | \n
Well-watered | \n5.2 ± 0.6 | \n0.62 ± 0.021 | \n
“Dark”" respiration, RD, and operating quantum efficiency of primary photochemistry in Photosystem II, ФPSII, measured in leaves of well-watered and moderately drought-stressed cotton genotype Navbakhor.
Response of the photosynthesis, AG, electron transport rate, ETR, and photorespiration, estimated as ETR/4-AG, to light intensity (PPFD) in leaves of the cotton genotype Navbakhor grown in well-watered (closed symbols) and moderately drought-stressed (open symbols) conditions in the field.
The light response of ETR and photosynthesis measured in plants of Navbakhor of the two treatments was similar to the CO2 response (Figure 5). At low light intensities, most of the energy from the electron transport is utilized in photochemical reactions, and with increasing of light intensity, more and more portion of this energy is spent for photorespiration. However, the increase in ETR induced by drought stress in light response was less expressed than that in CO2 response, particularly at higher intensities. Considerable variations of photosynthesis in different replications comparable with its difference between the treatments may be attributed to diurnal changes of stomatal conductance, gs, which can induce relevant changes in photosynthesis [57]. In view of tightly links between stomatal conductance and photosynthesis, and efficiency of primary reactions of photosynthesis remains constant, the changes in stomatal conductivity during the day may bring about considerable changes in photosynthesis [58]. In this case, the sum of photosynthesis and photorespiration, as measured using the ETR/4, is not constant, but varies during the day.
\nLight response of the chlorophyll fluorescence parameters: quantum efficiency of photochemistry in Photosystem II, ФPSII, photochemical quenching factor, qp, and non-photochemical quenching, NPQ, in leaves of the cotton genotype Navbakhor grown in well-watered (closed symbols) and moderately drought-stressed (open symbols) conditions in the field.
In the Figure 6 are shown the light response of the three key fluorescence parameters, operating quantum efficiency of photochemistry, ФPSII, photochemical quenching factor, qp, and non-photochemical quenching, NPQ, determined in leaves of well-watered and moderately drought-stressed cotton genotype Navbakhor. As shown from the figure, at low and moderate light intensities, PPFD < 800 μmol m-2 s-1, ФPSII in drought-stressed plants was higher than in well-watered plants, whereas qp was the same and near to its maximum. However, with increase of light intensity, ФPSII and qp decrease with increments, which are higher in drought-stressed plants. And finally, at PPFD > 800 μmol m-2 s-1, both ФPSII and qp become lower in drought-stressed plants in comparison with well-watered plants. What concerns to NPQ, it is negligibly low at low intensities in both treatments but increases rapidly at moderate and high intensities and under drought stress. So, increasing light intensity activates photosynthetic performance of plants. At low and moderate intensities, when the plant photosynthetic apparatus copes with coming light energy, the efficiency of photosynthetic conversion of light energy is very high, when photochemical quenching factor is near to its maximum and non-photochemical quenching is negligibly low. Long-term drought stress due to stomatal and non-stomatal limitations to photosynthesis induces enhancement of photorespiration as an alternative sink for transported electrons in reaction centers of photosynthesis. However, further increase of light intensity increases non-photochemical quenching, and in drought-stressed plants, it is higher than in well-watered ones. This causes faster decrease of ФPSII and qp in drought-stressed plants.
\nExperiments with the measurement of chlorophyll fluorescence and the gas-exchange in different cotton genotypes showed that under drought stress, CO2 uptake slightly decreases, while ETR increases considerably. Simultaneously measuring these two parameters of photosynthesis allowed us to estimate the magnitude of photorespiration in the plant leaves, assuming that changes in the ETR/4-AG reflect the changes in photorespiration. Photorespiration increases with increasing light intensity and decreasing CO2 concentration. Moderate drought stress noticeably increases the rate of photorespiration, which can be considered as a characteristic response of C3 plants to a drought [44].
\nLeaves of drought-stressed cotton plants displayed higher ФPSII and photorespiration at low and moderate light intensities, and non-photochemical quenching, NPQ, was stronger in drought-stressed plant than that in well-watered one. Obviously, higher levels of photorespiration in plant leaves during the drought stress exerts the “pressure” to the rate of electron flow and makes Photosystem II to operate with higher efficiency.
\nThe photosynthetic apparatus of plants supports higher performance of electron transport chain through enhancement of quantum efficiency of photochemistry in Photosystem II under drought stress. The accumulated energy in this state of over-excitation may be utilized in enhanced photorespiration. This protective reaction of the plant photosynthetic apparatus to drought stress has different magnitude depending on its drought tolerance. Field measurements of the chlorophyll fluorescence parameters simultaneously with morpho-physiological indicators of the cotton genotypes studied have displayed direct correlations between these parameters under drought stress. These correlations together with possible calibration of chlorophyll fluorescence parameters by photoacoustic characteristics determined at application of low-frequency-modulated light to plant leaves give new opportunities in monitoring of drought tolerance of various cotton genotypes in the field.
\nThe authors thank Dr. A. Massacci from the Institute of Agro-environmental and Forest Biology, CNR, Roma, Italy, and Dr. Y. Fracheboud and Dr. J. Leipner from the Institute of Plant Sciences, ETH, Zurich, Switzerland, for fruitful discussions on the photorespiration mechanisms in plants.
\nOrchids (family Orchidaceae) being iconic are at the front line of extinction, with 17,000–35,000 species distributed globally and are under threat [1, 2, 3]. The family is cosmopolitan in its distribution, but the genera and species are highly endemic [4]. In the Orchidaceae, greater levels of ecological specializations associated with global climate change, have a direct impact on the species diversity and levels of threat, to the extent that many terrestrial orchids in temperate regions have become extinct.
\nAustralia is rich in terrestrial orchid diversity (82%) with approximately 115 genera. The Southwest Australia Floristic region (SWAFR) is among 25 hotspots of biodiversity globally [5]. They can be found in a wide range of habitats across the continent and are usually categorized as epiphytes, lithophytes, and terrestrials, where epiphytes and lithophytes are mostly distributed in the warm and moist regions of tropics (18%) while few species are found in temperate regions of eastern Victoria and Tasmania [5]. They are mostly found in sclerophyll open forests and swampy coastal scrub lands. They grow on the ground especially in open habitats such as grasslands, heathlands and forest floors with low annual rainfall, showing seasonal changes and are mostly distributed in the southern temperate zones of Australia which have a Mediterranean climate. Most of the orchids growing in these temperate regions are deciduous, surviving climate extremes beneath the soil surface by undergoing dormancy [6].
\nThey usually have subterranean fleshy thick tubers or tuberoids that store nutrients during dormancy. Some of the most common terrestrial orchid genera found in Australia are, Caladenia (Spider orchids), Pterostylis (Greenhoods), Diuris (Donkey orchid), Acianthus (Mosquito orchid), Prasophyllum, Thelymitra (Sun orchids), Microtis and Glossodia (Figure 1) [5]. Caladenia’s are (spider orchids) endemic to Australia and represent one of the extraordinary terrestrial orchids with a large number of threatened and rare taxa [6]. In total there are 132 species of spider orchids which are mostly distributed throughout southern Australia.
\nAustralian terrestrial orchid species, (a) Caladenia spp. (b) Pterostylis spp. (c) Glossodia spp. (d) Corybas spp. (e) Diuris spp. (f) Acianthus spp.
From the ecological point of view, these orchids could act as ecological indicators of a healthy environment [7]. Due to their complex interactions with pollinators, fungal endophytes, and associated host trees, their conservation involves challenges at species-specific levels. These challenges are mostly linked to their habitat destruction and fragmentation, land use, climate change and unsustainable exploitation of biodiversity [8, 9]. Also, most of the terrestrial orchids of Australia, are continuously encountered by inappropriate fire regimes at different developmental stages of its life cycle, and places 74% of threatened orchid species at risk of extinction [10, 11, 12]. Recently, the impact of nature-based tourism has also been reported as a major threat to the decline of threatened orchid populations in the wild in South Australia [10]. Due to these factors, the survival of various species from this genus is at risk and thus considerable effort is required from scientists and conservation practitioners to overcome these challenges of the twenty-first century. However, with the ability to use current novel technologies in orchid biology greater than ever before, we can help them conserve for future generations.
\nAustralian soils are generally deficient in nutrients, which have mostly leached out of the sandy soils (podzols) over many millions of years [13]. In a fire-prone Australian ecosystem, fungi can have a major influence on surrounding biota and play an essential role in maintaining the healthy ecosystems as effective symbiotic partners, decomposers, nutrient cyclers and are a source of food for various organisms. The top horizon of organic matter is the major source of carbon (C), nitrogen (N) and phosphorus (P). In most coarse-rooted plants like orchids, with a poorly developed root system, mineral nutrition is highly dependent on mycorrhizal uptake of essential elements such as N and P from their surroundings [14]. Orchid mycorrhizal fungi (OMF) present in these nutrient-depleted soils are likely to derive their nutrition from the organic matter (dead roots, exoskeletons, leaves and wood in a litter), which holds various types of complex compounds. These complex molecules are further degraded into simpler forms by the activity of these mycorrhizal fungi and other microorganisms. C is usually available in complex forms such as cellulose, hemicelluloses, pectin and lignin, as well as simple soluble breakdown products from these complex polymers. Also, availability of N is usually in the form of organic peptides, proteins and amino acids and as inorganic ammonium and nitrate ions whereas phosphorus is mostly available as organic compounds such as phytic acid and sparsely available as inorganic ions such a PO4\n3−, HPO4\n2− and H2PO4.
\nThe ability of OMF to assimilate various C, N and P compounds as compared to other ericoid mycorrhizal (ERM) and ectomycorrhizal (ECM) fungi, has been studied previously but information available until now is fragmentary [15, 16, 17, 18]. It is very important to understand the nutritional physiology of endophytes associated with terrestrial orchid species while considering any recovery plans for propagation, management, conservation and restoration of Australian endangered orchid species in wild. Therefore, in this chapter, we have discussed in general about orchid endophytes and their saprophytic ability in digesting complex resources, confined to its litter prone, open and well-drained podzol sites.
\nAll orchids share obligate relationships with their endophytes, from early seed germination stages to later development of seedlings and mature plants. Endophytes are commonly found inside the healthy tissues of orchid roots as bacterial and fungal endophytes without causing any symptoms of a disease. In this mutualism, fungus provides water and mineral nutrition to the host plant which in turn provides photosynthetically fixed carbon back to its fungal partner [4], phenomenon which is commonly found in fully autotrophic orchid species [19] as compared to completely mycoheterotrophic (MH) and partially MH orchid(Mixotrophic)species [20, 21, 22].
\nPhysiology of orchid seed germination is one of the interesting phenomena of nature and therefore must enter symbiotic interaction with a species-specific symbiont for appropriate germination. All orchid species are MH in their early stages of seed development, where orchids obtain their nutrition in the form of minerals, salts, water and carbon supply from their fungal symbionts at least in their initial seed germination stages [23]. Once the fungus invades the minute orchid seeds (having low endosperm reserves) it kicks starts the germination process, eventually giving rise to an undifferentiated mass of cells known as protocorms. However, this mutual symbiosis between the host and its fungal partner has not been understood completely, it seems that orchid is having a complete control over-regulating the degree and level of these associations. Germination and vegetative propagation in their natural environment is very slow with a rate of <5% [24]. The distribution of orchids and their diversity is dependent on the availability of their fungal symbionts and thus understanding orchid mycorrhizal symbiosis is a key factor to conserve orchids.
\nVarious orchid species have heterobasidiomycetes as their symbionts [25]. The complex assemblage of fungi associated with orchids consists of Agaricomycetes (=Hymenomycetes) taxa [26]. OMF was traditionally classified as anamorphic form-genus (imperfect stage) Rhizoctonia (=Epulorhiza). These correspond to three distantly related basidiomycetous lineages forming teleomorphic genera, including Ceratobasidiaceae, Tulasnellaceae and Serendipitaceae [27]. Although the OMF is well known for its saprophytic abilities [4] they may be found widely as endophytes in non-orchid roots [28] without forming any symptoms of infection.
\nRecently, a range of mycorrhizal fungi has been found associated with different orchid species, apart from their long evolutionary history of associations with rhizoctonias [26]. OMF studies on MH and mixotrophic orchid species have shown a huge diversity of ectomycorrhizal fungi [23], including saprotrophic fungi from Mycenaceae and Psathyrellaceae and some ascomycete taxa, which suggests that depending upon their host, same fungi could have a potential to form dual associations in nature. Photosynthetic orchids can also associate with a variety of taxa, including Psathyrellaceae and saprotrophic fungal species [29].
\nMembers of Tulasnellaceae, Serendipitaceae (Sebacinales clade B) and Ceratobasidiaceae are well known for their endophytic [30] and saprophytic abilities [31] with few exceptions from Ceratobasidiaceae where some species are plant-parasitic [27]. Serendipita indica is one of the well-studied, root endophyte models and is indeed found mycorrhizal with orchid roots [32]. Fungi in the Serendipitaceae are involved in a wide range of mycorrhizal associations such as ectomycorrhizas, ericoid mycorrhizas, orchid mycorrhizas and even liverworts (Jungermannioid mycorrhizas) [26, 33, 34, 35]. Phylogenetically the Serendipitaceae (formerly called Order Sebacinales) is grouped into two clades: A and B [36]. Clade A species constitutes jelly fungi, having a saprophytic ability through which they can obtain their nutritional demands from wood and other surrounding litter present in their habitat, while Clade B species are common endophytes of underground plant organs [37]. The fungi from Clade B are usually associated with orchids, for example, Caladenia species in Australia, are also associated with ericoid roots, though without having any proof of functional symbiosis so far [33]. There are studies which have shown presence of basidiomycetous hyphae with septal pores on and in sections of ericoid plants by transmission electron microscopy (TEM) whereas, there is an evidence of DNA sequences from the nuclear ribosomal internal transcribed spacer (ITS) region from ericoid roots that grouped within Serendipita group B and contained identical sequences to those from Serendipita vermifera isolates from Australian green orchids [4]. S. vermifera [30] in group B [38], has a confirmed mycorrhizal relationship with some green orchids, e.g. in Caladenia and Glossodia species and is the most common OMF found associated to these taxa [39, 40, 41, 42].
\nTraditional approaches were commonly used to identify these fungal endophytes of orchids by isolating the pelotons from the orchid tissues and maintaining them as pure cultures. Mycelia are mostly present as anamorphs and the orchid endophytes are commonly identified based on their morphological (hyphal walls), anatomical differences (spore formation and nucleus number) and anastomosis behavior [43] by using optical, scanning and electron microscopy. Most form chains of small ovoid-globular monilioid cells. Recently, several molecular approaches are extensively used to delimit the fungal endophytes of orchids (Ceratobasidium, Tulasnella and Rhizoctonia = Serendipita) which are well known for their poor taxonomy [44, 45].
\n\nRhizoctonia is remarkable in some characteristics as they branch out at acute angles when young but at right angles to the main axis at maturity, mainly constricting at the point of branching [46]. Fungi grown from pelotons usually form ovoid monilioid cells without having any clamp connections or conidia in a culture that limits their identification through morphological methods [40]. Rhizoctonia, is traditionally characterized on the basis of anastomosis groupings including the pathogenic strains [47]. Rhizoctonia species are separated on the basis of the ultrastructure of the number of nuclei in each cell and the septa, and on the basis of what can be categorized as uninucleate, binucleate or multinucleate [48]. The commonly isolated Rhizoctonia fungi from terrestrial orchid species are within the anamorphic genera Ceratorhiza, Moniliopsis, Thanatephorus and Epulorhiza.
\nThe commonly isolated Rhizoctonia fungi from terrestrial orchids are species within the teleomorphic genera, Ceratobasidium, Tulasnella and Serendipita. Imperfect stages of Rhizoctonia are commonly found in various chlorophyllous orchids. For most Australian green orchids, in-vitro cultures produce only monilioid cells but Warcup and Talbot obtained teleomorphic stages on Rhizoctonia isolates in culture [40, 41, 49], an achievement not replicated by many researchers despite numerous attempts. Because of this, the systematics of Rhizoctonia-type OMF has been studied using both morphological [43, 46] and molecular approaches [25, 38, 44, 45, 50], which have suggested various anamorphs and teleomorphs for this polyphyletic group.
\nThe nutrition of orchids is closely tied to the nutrition of their basidiomycetous OMF. The fungal symbionts provide essential nutrients for the establishment of orchid seedlings from obligate MH stage to mixotrophic to fully autotrophic stages of their development. They can obtain their nutrition as saprophytes, by breaking down wood and other litter in their habitats or by tripartite symbiosis, in which the OMF is also ectomycorrhizal on the roots of the surrounding higher plants. Both result in networks of hyphae linking the host plants to various habitats.
\nIn general, achlorophyllous orchids mostly have mycorrhizal associations with homobasidiomycete fungi in the Cantharellales, Thelephorales, Agaricales, Serendipitaceae, Hymenochaetales, and Russulales, which are also pathogenic and ectomycorrhizal on higher plants [51]. In MH orchids, the fungi often form tripartite relationships, being ectomycorrhizal with woody plants and endomycorrhizal with orchids [23, 52, 53] where, transfer of carbon has been shown from the woody plants to the orchid [52, 54]. Fungal symbionts of MH orchids have three lifestyles: ectomycorrhizal (ECM), e.g. Corallorhiza-Russulaceae, parasitic (pathogenic), e.g. Gastrodia—Armillaria species, and saprophytic, e.g. Epipogium—Coprinus and Psathyrella species. Various achlorophyllous orchids such as Gastrodia confusa [55], G. elata [56], Epipogium roseum [57] and Fulophis zollingeri [58], are associated with many species of saprophytic wood- and litter- decaying fungi. Earlier studies have provided morphological and ultrastructural evidence that fungi from the Serendipitaceae formed ectomycorrhiza with Corylus avellana and Carpinus betulus [25] suggesting that common mycorrhizal networks (CMNs) are likely to be found in the plant communities where MH orchids are distributed in the close vicinity of ectomycorrhizal higher plants where they can obtain their nutrition through a tripartite relationship. Molecular studies have also shown the presence of Serendipita species on MH orchids such as Hexalectris spicata and Neottia nidus avis, suggesting that, if Serendipita is ubiquitous in its distribution, it is of interest to elucidate any functional symbiosis with ECM on higher plants.
\nChlorophyllous orchids mostly have mycorrhizal associations with fungi in the Rhizoctonia alliance, in the Cantharellales and Sebacinales (Serendipita Group B), with sexual stages in the Ceratobasidiaceae, Serendipitaceae and Tulasnellaceae [4]. Some of the Rhizoctonia species in the Ceratobasidiaceae are also plant pathogens of crops [4]. Fungal endophytes from the Serendipita group are common among photosynthetic orchids, e.g. Caladenia [42, 59] and non-photosynthetic terrestrial orchids, e.g. Neottia [53, 60, 61]. They constitute two major groups: A and B [36]. Group B forms mycorrhizae with green orchids while group A is generally associated with ECM and some non-photosynthetic orchids [26].
\nFungal specificity is common in Australian terrestrial orchids [39, 62]. Taxonomically related groups of Australian terrestrial orchid genera are associated with taxonomically related groups of fungi. Both achlorophyllous and chlorophyllous orchid species can have fungal specificity [57, 63] but is more remarkable among heterotrophic orchid species [64]. By contrast, chlorophyllous photosynthetic mycorrhizal plants are said to be generalists in their associations with mycorrhizal fungi [4], though there is evidence of specificity at the species and strain level in Australian OMF and their host orchids, especially Caladenia [17, 65].
\nMost common genera of seasonally dormant terrestrial orchids in Australia belong to the Tribe Diurideae; within this, genera in the Sub-tribe Prasophyllinae usually associate with Ceratobasidium, those in the Caladeniinae with Serendipita, and most of those in the Diuridinae, Drakaeinae and Thelymitrinae associate with Tulasnella. Genera in the Acianthinae and the Megastylidinae associate with Serendipita and/or Tulasnella, e.g. Thelymitra. calospora and Lyperanthus nigricans associated with a wide range of endophytes. Also, variations in seed germination rates with fungal isolates of T. calospora were noticed in Diuris species [39]. However, within these general relationships, fungal strain, seed and fungal provenance play an important role; specificity varies from high in C. tentaculata, in which seed and fungal provenance both varied seed germination significantly, to low, in which more than one species of Tulasnella stimulated germination in Thelymitra [39].
\nOMF effectiveness leads to increased seed germination rate and fitness of orchids [66]. Specificity can be strictly restricted to the early seed germination stages of orchid or involve the compatibility of the fungal symbiont with the orchid throughout later stages [67]. Masuhara and Katsuya [62] has expanded fungal specificity into “potential and ecological specificity” whereas, earlier in-situ seed baiting studies from endangered and common orchids have shown distributions of OMF independent of their host orchids [68], suggesting that the patchiness of many orchids is not due to patchiness of their compatible species.
\nPrevious research has also shown fungal specificity with particular orchid species during germination stages; for example, Neottia nidus-avis needs a specific Serendipita-like fungus to germinate [61]. Fungal specificity and effectiveness vary with individual isolates associated with the host orchid species for example, OMF isolated from Caladenia species were effective in germinating seeds of both Caladenia and Glossodia as compared to Eriochilus cucullatus and Acianthus reniformis [39]. These seed germination tests, under in-vitro conditions, over-estimate the potential of OMF isolates to form effective symbioses with orchid species, and results in a failure of symbiosis during later stages of orchid development thereby parasitizing the host plant [69]. Also, it does not explain the fungal switching that has been recorded during the lifetime of an orchid in the wild [70].
\nDecomposition of organic materials present in the form of dead decaying material such as fallen leaves, litter, hair, exoskeletons and any other kind of waste product from plants or animals is the main source of carbon compounds available.
\nIn forest ecosystems, mineral nutrients in the form of P and N are mostly locked within living organisms or in the organic layer of soil. The distribution of these resources is heterogeneous in terms of space and time [71]. Access to nutrients by the host plant depends on the ability of the mycorrhizal fungi to mineralize the available organic nutrients to intermediate and soluble forms and then mobilize them to the host plant [72]. OMF can grow freely in the environment and have an ability to sustain itself without its host [21]. Mycelium is the predominant vegetative form among the basidiomycetes, comprising interconnected hyphae [71]. Fungal foraging for the uptake of minerals and other resources that are interlocked in the organic layer of the soil largely takes place at hyphal tips. Fungal hyphae have a large surface to volume ratios and secrete enzymes that digest extracellular organic resources, which are further translocated to a sink in the form of simple soluble compounds [73]. From the nutrient-deprived ecosystems of Australia, very limited information is available on the ability of OMF to utilize various C, N and P sources from the complex litter present on the forest floors.
\nFor successful symbiotic interactions, efficient utilization of nutrients by the fungal partners is a prerequisite. In most mycorrhizal associations, photosynthetic products are transferred from an autotrophic host plant to a heterotrophic fungal partner, while the mineral nutrients obtained from the soil move in the opposite direction [74]. By contrast, in mycorrhizae of the photosynthetic orchids, the flow of nutrients is bidirectional, at least in some orchids [19]. In orchids, nutrient uptake into OMF occurs mainly through the acquisition of soluble nutrients from the decay of organic litter present in the top 4–12 cm of topsoil [73]. Information on the types of soluble carbon sources OMF can utilize from the environment and their host plants are very limited.
\nFew studies have reported inter- and intra- specific variations in utilization of substrates among orchid and ericoid mycorrhizal fungi from the same habitat [16, 18]. Also, Wright et al. [17] provided evidence of genetic and functional diversity among OMF isolates of C. tentaculata that varied in germination rates and utilization of some C and N sources. Unlike many ECM basidiomycetes, OMF has also retained the genes for the breakdown of these complex carbon compounds [31]. Understanding the nutritional roles of OMF may explain the diversity noticed among fungal isolates, from even single orchid plants in rates of symbiotic seed germination in vitro. However, in most cases, only one symbiotically effective fungus was examined from each orchid species from their habitat despite, a large number of fungal variations commonly isolated from even single plants. The symbiotic effectiveness of these isolates might vary with their ability to take up and utilize various carbon sources from their surroundings, an aspect that has not been studied so far.
\nDuring the early stages of orchid seed development, both achlorophyllous and fully autotrophic orchid species lack their ability to synthesize carbohydrates and the only available source of carbon and nitrogen to these plants is through OMF associated to them. One of the common assumptions so far in the orchid biology is that OMF can obtain its nutrition by digesting the litter components present on the forest floors and there has not been much evidence of their ability to grow on these litter components apart from few studies [15, 16, 17, 18, 75]. There are reports where orchids are found in close vicinity of moss lying on the forest floors but there is no scientific evidence showing the presence of OMF on them or surrounding litter [15]. S. vermifera complex is mostly root biotrophic [37] and is associated with Caladenia species that is believed to be saprotrophic, at least as far as the fungi isolated from the Australian orchids is concerned.
\nIn their natural habitat’s orchids are commonly surrounded by litter such as bark, leaves and wood. During ex-situ measures for orchid conservation, these components have been extensively used as mulch in the pots of orchids to retain proper moisture levels. In Australia, Casuarina branchlets are commonly used as a source of mulch for re-emergence and growth of orchids during ex-situ conservation measures based on an assumption that they help orchid leaves from drying up but there is a possibility that these litter components on their break down may help them in the nutrition of the OMF and hence the orchid growth [75]. Recently, Mehra et al. [15] have validated their use in ex-situ cultivations by showing the amounts of fungal biomass produced on natural and semi-purified substrates from various endangered and common Caladenia species under in-vitro conditions.
\nNutrient-poor soils are inadequate in their microbial decomposition rates and the dead organic matter present on the soil is mostly utilized by decomposer fungi [76]. Litter constituting bark, wood, and leaves have biopolymers such as chitin, pectin, lignin, cellulose, hemicellulose and contain complex cell wall polysaccharides along with chitin of fungal and invertebrate origin. Most of this organic waste is in the form of plant cell wall components which constitutes 90% of plant cell wall components, having three major polysaccharides: cellulose, hemicelluloses and pectin [77]. Of these, cellulose and pectin are key components of organic substrates in vegetation and are an important source of nutrients for ectomycorrhizal fungi [78]. Also, chitin is the main polysaccharide found in fungal cell walls and invertebrate exoskeletons [79] having significant quantities of nitrogen. These complex biopolymers are degraded enzymatically into simpler water-soluble forms of sugar through saprotrophic or mycorrhizal fungi reflecting their saprophytic ability which can be indirectly related to the survival of their host plant. For the survival of the host plant in wild, its nutritional demands for carbon and energy are met by the decomposition of this organic content present in the environment by OMF at the same site. Little information is available on the saprophytic behavior of OMF and more research is required to understand the nutritional physiology of both the partners by having a complete understanding of the role of OMF in decomposing the organic matter present in the ecosystem.
\nThe decomposition of organic matter by saprotrophic basidiomycetes is a complex mechanism and does involve the participation of various enzymes and reactions. Saprophytic fungi stand apart from other organisms in their ability to decompose non-protein sources [73]. Various chlorophyllous and achlorophyllous orchid species are associated with saprophytic fungi from species of Rhizoctonia and Epulorhiza [80]. Utilization of these complex compounds in a litter is associated with the activity or production of extracellular enzymes (endo- or exo-) in basidiomyceteous fungi. These complex sources of carbon are degraded into their simpler forms through the activity of hydrolytic enzymes. Various litter components require a different set of enzymes for decomposition to occur such as cellobiohydrolases, Endo-1,4-β glucanases, and 1,4-β-glucosidases which effectively decompose cellulose to cellobiose. β-glucosidases then convert cellobiose to glucose.
\nHemicelluloses are the second most abundant, heterogeneous polysaccharides present in the plant cell walls and comprise branched polymers of 500–3000 C5 or C6 sugars [81]. Lignin and plant cell wall polysaccharides (hemicellulose) interact with cellulose fibers to strengthen plant cell walls. Pectinases are widely produced by plant pathogens and endopolygalacturonase is one of the major enzymes involved in pathogenesis produced by a large number of pathogens such as Rhiizoctonia solani [82], Phytophthora infestans and Verticillium species [83]. Several pathogenic fungi degrade pectin and the release of these enzymes allows them to infect their host plant under favorable conditions but activates the cascade of defense reactions in plant cells [84].
\nRecent studies on OMF from Australian orchids, in the genera Caladenia, Diuris, Drakaea and Pterostylis, have shown utilization of pectin as a sole carbon source, resulting in the production of fungal biomass ranging from greater than to less than that on xylan [16]. Several extracellular enzymes, such as dehydrogenases and oxidases from the mycelium, are involved in wood-lignin decomposition and have the potential to utilize all major constituents of litter [81]. Microbial decomposition in heathland soils is a slow process [85] and the penetration of the resource is important [86]. Most wood-associated decay reactions occur close to fungal hyphae due to limited amounts of diffused enzymes [81] and lignocellulose-degrading units in the cell walls [87]. Burnett [88] proposed that enzyme secretion may occur in different areas of the apical region and these findings were further supported by experimental evidence in Neurospora crassa, where structural and physiological differences in the hyphal cell wall at the apical region contributed to the variation in secretion and retention of exoenzymes in the wall.
\nIn many ecosystems, most of the nutrients are locked up in organic compounds, soil microflora and microfauna. Organic macromolecules present in the soil are degraded to intermediate forms through the saprophytic ability of decomposers adding up to higher decay rates in the soil [89]. Some of the complex compounds in the form of cellulose, hemicelluloses (xylans and arabinoxylans), starch and pectin are degraded to soluble intermediate forms such as oligosaccharides, disaccharides, cellobiose, xylobiose and maltose which are finally broken down to their soluble breakdown products such as glucose, mannitol, trehalose, arabinose, galactose, mannose, xylose, rhamnose and glucuronic acid.
\nOn penetrating a substrate, fungi decompose it and absorb its nutrients. The available nutrients help the fungus to grow and proliferate until the nutrients are depleted and fungus becomes dormant. In nature, succession starts at this point and other species feed on the remains. Succession in microorganisms is very important in completely digesting complex carbon sources to simple soluble compounds. The C:N ratio plays a vital role in determining microbial growth and the amount of decomposition taking place. Inter-relationships are sometimes antagonistic, with exploitation, antibiosis and competition being very common [89]. An average of 30–40% of C from decomposed substratum is assimilated by the fungi under favorable conditions [89].
\nOMF, as saprophytes, break down these complex macromolecules and transfer the intermediate and final soluble products to their hosts. The fungal partner increases the efficiency of the host plant in acquiring C, N and P from litter and soil.
\nSo, it is important to understand the ability of OMF to utilize soluble carbon sources. Fungi break down complex molecules into intermediate and then simpler water-soluble forms. These soluble forms are then assimilated and used in metabolic pathways, or liberated as free metabolites, to be used by the OMF or competitive microorganisms, and may be subsequently transferred to the host plants.
\nSome of the soluble compounds released on the digestion of complex carbon sources are simpler soluble forms of sugars in the form of monosaccharides and disaccharides. OMF vary in their absorption of nutrients from the soil, similar to other mycorrhizal fungi. The ability of OMF to utilize a range of soluble carbon compounds has been studied previously but information available is fragmentary if compared to other mycorrhizal groups such as ERM and ECM fungi. Earlier physiological studies have stated that OMF metabolize sugars through an activity of enzymes such as and maltases and diastase-invertases [90]. There is little information available on the activity of enzymes and transporters involved in OM symbioses, but soluble carbon sources are likely to be transported rapidly to both pelotons and orchid cells which are later used in metabolism. Moreover, few studies have demonstrated the translocation and hydrolysis of the disaccharide sugar trehalose at the interface of the symbionts in MH orchids [91, 92]. Isotopic studies have shown a two-way transfer of carbon between the OMF and the orchid host [91, 93, 94] and it has recently been suggested that C and N containing compounds (derived from glucose and ammonium nitrate) are transferred from both senescent and live pelotons in Spiranthes sinensis–Ceratobasidium sp. AG-1 symbiosis in vitro [95].
\nTo understand the potential of OMF to use soluble carbon sources requires their growth on a range of single carbon sources followed by measurement of their growth as fungal biomass. Research on Australian OMF has generally shown utilization of various soluble carbon sources such as the C5 arabinose, C6 glucose, C12 sucrose and cellobiose, and C(n) cellulose (as CMC), xylan, and pectin, and tannic acid [16, 17, 18]. Biomass on soluble carbon sources can be easily quantified by measuring the dry weight of mycelium and subtracting the biomass of controls from all the treatments, as used by Midgley et al. [16], Wright et al. [17] and Nurfadilah et al. [18] and Mehra et al. [75]. More recent studies have shown trends in utilization patterns of carbon sources across four fungal taxa from the Rhizoctonia alliance (Ceratobasidium, Rhizoctonia, Tulasnella, and Serendipita). OMF from these taxa produced large biomass on xylan, glucose, cellobiose, cellulose, pectin, and to some extent CMC, and the least fungal biomass was reported in all for tannic acid [18]. In studies on OMF from Australian orchids in the genera Caladenia, Diuris, Drakaea and Pterostylis, xylan consistently produced the greatest growth, often exceeding that on glucose [16, 17, 18].
\nFor the establishment of balanced symbiosis between two partners more research using similar methods is required to determine the nutritional preferences displayed by OMF from other Australian terrestrial orchid species. The ability of an OMF to compete for and use soluble carbon compounds from sources external to the orchid may reflect the ability of its host orchid to survive and thrive.
\nN present in the soil litter is typically found in the form of inorganic N (nitrates and ammonium) and organic N. Organic N comprises a large fraction of Australian litter but its utilization by OMF has been poorly studied. In the natural environment, amides and amino acids are easily accessible to the OMF, external to the orchid as a result of a litter breakdown and internally in the orchid as a result of plant metabolism.
\nThe utilization of a wide range of organic and inorganic forms of nitrogen by OMF suggests their specificity of enzymes to hydrolyze complex forms of amides and peptides into simpler soluble organic N sources that are directly absorbed by OMF. The uptake and transfer of N by OMF has already been reported previously for northern hemisphere OMF [20, 96, 97] whereas, Cameron et al. [93] provided direct evidence of uptake and transfer of organic N through Ceratobasidium cornigerum (from Goodyera repens) by double-labeling of amino acid glycine. Recently, studies have also shown a transfer of N from the soil and through tripartite relationships by a single OMF of MH orchid, Rhizanthella gardneri [98]. Most recently, the uptake and transport of nitrogen from NH4NO3 was inferred from isotopic enrichment of 15N in the pelotons and uninfected cells of Spiranthes sinensis protocorms using ultra-high spatial resolution secondary ion mass spectrometry (SIMS) [95]. With inorganic N sources, most authors reported greater utilization of NH4\n+ than NO3\n− in OMF strains of Tulasnella (one strain, C. flava) and Serendipita (six strains, C. tentaculata) whereas, many of these did not utilize nitrate [17, 18]. With organic sources, most OMF were capable of utilizing C3 alanine, C4 aspartic acid and/or asparagine, C5 glutamic acid and C6 arginine well as compared to C5 proline and C6 histidine which were poorly utilized [17, 18, 99]. Few OMF utilized C2 glycine well and others poorly; the latter included an isolate from C. flava [18]. In addition, only two out of six OMF from Australian Pterostylis species utilized tryptophan [16]. Recently, research work on Australian endangered orchid species (C. fulva) has shown that one of the symbiotically effective isolates, utilized most of the N sources with minimal variations in their biomass in contrary to the ineffective isolate under in-vitro conditions. The reason suggested for this was that it would affect their competition, at both levels in the host plant (internal/external) whereby, an ineffective isolate can successfully outcompete the effective isolate and its host, leading to chlorosis before the death of an earlier surviving orchid seedling [15].
\nMost Australian soils are ancient and are phosphorus-deprived, as most of it has been leached out over time [100]. Along with N, it is one of the major limiting factors for plant growth. In soil, it is present in two major forms: inorganic P (Pi) in the form of phosphates where they are present in the form of scarcely available complexes [101] and mineral and organic phosphorus (Po) as phosphate diesters, phosphate monoesters and inositol phosphates [100] where they are low in orthophosphate levels [102]. In natural environments, fungi degrade organic phosphorus compounds present in the dead matter but organic phosphorus locked in humus-rich forest soils is not easily accessible [100, 103]. Inorganic phosphorus has low solubility and is present in three main fractions: soil solution (dissolved phosphates), a labile pool (phosphates adsorbed to surfaces) and a non-labile pool (metal phosphates) [104].
\nPlants cannot utilize organic phosphates as they only have access to soluble phosphates and can readily absorb them [104]. Mycorrhizal associations can overcome nutrient limitations to plant growth by increasing the availability of phosphorus. Fungi can release phosphorus into the soil solution from organic phosphates with the help of phosphatases, thereby providing access for plants to otherwise insoluble forms of phosphorus [105]. The greater availability of phosphorus to the mycorrhizal plant host is dependent on the ability of its symbiont to absorb and translocate inorganic phosphates to the host roots and to access the forms of phosphorus ‘locked up’ in organic debris [106, 107]. Fungi can store phosphorus in their vacuoles as polyphosphate chains or as condensed phosphate [108].
\nTerrestrial orchid habitats are nutrient-deprived in Australia and leaf litter is among one of the major phosphorus sources available to OMF [100], through its richness in the cyclic phytic acid (inositol hexaphosphate, IP6, inositol polyphosphate), the main form of phosphorus storage in plants. In orchids it is assumed that mycorrhizal associations benefit the host plant by increasing the uptake of phosphorus. Earlier studies have reported the secretion of acid phosphatases by fungi in pure cultures [43]. The transfer of organic phosphorus in young protocorms of orchids through mycorrhizal fungi was first demonstrated by Smith [109] whereas, the uptake of inorganic phosphorus in mycorrhizal adult seedlings of Goodyera repens has been reported previously. Whilst, the utilization of organic phosphorus was demonstrated by Smith and Read [4] through the hydrolysis of organic compounds with a release of inorganic phosphorus (Pi). So far, there are few studies on the utilization of various forms of phosphorus by OMF in contrast to extensive work done on other mycorrhizae. A recent study by Nurfadilah et al. [18] showed that OMF from four genera of Australian orchids produced greater biomass with inorganic phosphate than DNA and with intermediate levels in case of phytic acid.
\nFungal preferences for specific carbon sources from the heterogeneous and unstable distribution of the substrates on forest floors might suggest that different stages of host plant development may have a preference for different organic substrates, for example, the abundance and presence of orchid seedlings (Tipularia discolor) near decaying logs in specified habitats as opposed to their absence near-adult flowering individuals [43] suggests that OMF does have preferences for their carbon sources, which could therefore explains their patchy distribution in the environment. The relative lack of utilization of some soluble components likely to be generated, may offer opportunities and niches for other fungi and microorganisms in general. OMF must compete not only with one another but also with other mycorrhizal and saprophyticic fungi for these resources, and for their breakdown products.
\nThe relative abilities of OMF from Australian endangered and common orchid species (Caladenia spp.) to grow on the breakdown products of litter may have some ecological implications for their orchid hosts in terms of their taxonomy and conservation status [75]. Similarly, Nurfadilah et al. [18] concluded that the OMF from rare and common orchid species has the same utilization profiles of soluble carbon sources, having slow and uncompetitive growth could explain the conservation status of its host orchid. The importance of these nutritional studies can be related to the patchy spatial distribution of OMF and their host orchids [110]. Previous in-vitro studies showed competition between orchid siblings for available resources through their OMF and there is a possibility that this could be true for the orchids growing in the wild [111, 112].
\nMehra et al. [75] showed that the OMF from various Caladenia species are differentiated not so much by different profiles of carbon sources utilized but by different rates of growth and final biomass. This suggests that threatened orchids contain OMF with relatively slow-growing and uncompetitive OMF compared with those from common orchids. It would be interesting to test this further by examining more OMF from a greater range of orchids. Also, Ceratobasidium species have rapid rates of growth compared with those of Serendipita and Tulasnella, the other two main OMF of Australian orchids, and it would be interesting to test these in direct competition in microcosms to see the effects on the survival of orchid seedlings of their respective hosts.
\nOrchids depend on their fungal endophytes for their nutritional demands, which is obligatory in its initial stages but may vary in adult green orchids, though they continue to harbor OMF in their underground organs. The forms of C, N, and P available to the OMF can determine their availability to the orchid host and can indirectly affect its conservation status. Thus, obtaining an effective symbiont is critical for an orchid’s survival and is absolutely a high priority in recovery plans for endangered species. In order to develop effective strategies for conservation of orchids, a large number of orchid taxa should be tested for their nutritional modes as a function of their habitat based partly on organic content using labeling techniques and isotopic fractionations. Also, future research should be focused on developing enzymatic profiles for OMF using sterilized natural substrates and insoluble carbon sources, which may augment our understanding of the role of OMF in the decomposition of organic matter in the ecosystem. Uptake of soluble carbon sources in OMF from terrestrial green orchids can be further investigated through radiotracer techniques through labeling and setting up small microcosm experiments. Tracing the translocation of external highly enriched carbon sources over a short period of time will provide evidence on the net transfers of different forms of carbon between the OMF and the orchid.
\nAuthor acknowledges all the valuable guidance provided by Professor Ann C Lawrie and Dr Fiona Coates from RMIT University, Melbourne, Australia.
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