Intertwined signatures of desiccation and drought tolerance in grasses
Jeremy PardoChing Man WaiHannah ChayChristine MaddenHenk W. M. HilhorstJill M. FarrantRobert VanBuren
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Abstract:
Grasses are among the most resilient plants, and some can survive prolonged desiccation in semiarid regions with seasonal rainfall. However, the genetic elements that distinguish grasses that are sensitive versus tolerant to extreme drying are largely unknown. Here, we leveraged comparative genomic approaches with the desiccation-tolerant grass Eragrostis nindensis and the related desiccation-sensitive cereal Eragrostis tef to identify changes underlying desiccation tolerance. These analyses were extended across C4 grasses and cereals to identify broader evolutionary conservation and divergence. Across diverse genomic datasets, we identified changes in chromatin architecture, methylation, gene duplications, and expression dynamics related to desiccation in E. nindensis . It was previously hypothesized that transcriptional rewiring of seed desiccation pathways confers vegetative desiccation tolerance. Here, we demonstrate that the majority of seed-dehydration–related genes showed similar expression patterns in leaves of both desiccation-tolerant and -sensitive species. However, we identified a small set of seed-related orthologs with expression specific to desiccation-tolerant species. This supports a broad role for seed-related genes, where many are involved in typical drought responses, with only a small subset of crucial genes specifically induced in desiccation-tolerant plants.Keywords:
Desiccation Tolerance
Eragrostis
Drought Tolerance
Recalcitrant seed
Grasses are among the most resilient plants, and some can survive prolonged desiccation in semiarid regions with seasonal rainfall. However, the genetic elements that distinguish grasses that are sensitive versus tolerant to extreme drying are largely unknown. Here, we leveraged comparative genomic approaches with the desiccation-tolerant grass Eragrostis nindensis and the related desiccation-sensitive cereal Eragrostis tef to identify changes underlying desiccation tolerance. These analyses were extended across C4 grasses and cereals to identify broader evolutionary conservation and divergence. Across diverse genomic datasets, we identified changes in chromatin architecture, methylation, gene duplications, and expression dynamics related to desiccation in E. nindensis . It was previously hypothesized that transcriptional rewiring of seed desiccation pathways confers vegetative desiccation tolerance. Here, we demonstrate that the majority of seed-dehydration–related genes showed similar expression patterns in leaves of both desiccation-tolerant and -sensitive species. However, we identified a small set of seed-related orthologs with expression specific to desiccation-tolerant species. This supports a broad role for seed-related genes, where many are involved in typical drought responses, with only a small subset of crucial genes specifically induced in desiccation-tolerant plants.
Desiccation Tolerance
Eragrostis
Drought Tolerance
Recalcitrant seed
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Abstract There are substantial scientific reports on the basic physiology and desiccation sensitivity of recalcitrant seeds, but ecological and evolutionary aspects of their biology have received scant attention. Recalcitrant seeds are shed hydrated, are desiccation sensitive and have a short lifespan. In vegetative tissue, desiccation sensitivity is probably the ancestral state, but tolerance is thought to have evolved early and a number of times independently. It is difficult to see evolutionary relationships among species producing recalcitrant seeds. However, it is suggested that early evolved seeds were desiccation sensitive and that desiccation tolerance is a derived characteristic. Desiccation sensitivity and short lifespan of recalcitrant seeds places constraints on the range of environmental conditions in which reproductive success can occur. Species producing recalcitrant seeds are common in humid tropical forests, where the seeds of climax species germinate and form a seedling bank, rather than contributing to the soil seed bank. However, there is a wide range in post‐shedding physiology among recalcitrant seed species, and recalcitrant seeds do occur in habitats with seasonal climates. Here, regeneration strategies may be more specialized.
Recalcitrant seed
Desiccation Tolerance
Climax
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Abstract Grasses are among the most resilient plants and some can survive prolonged desiccation in semi-arid regions with seasonal rainfall. This vegetative desiccation tolerance has arisen independently multiple times within the grass family, but the genetic elements that differentiate desiccation tolerant and sensitive grasses are largely unknown. Here we leveraged comparative genomic approaches with the resurrection grass Eragrostis nindensis and the closely related desiccation sensitive cereal Eragrostis tef to identify changes underlying desiccation tolerance. We extended the analyses to include the grasses maize, sorghum, rice, and the model desiccation tolerant grass Oropetium thomaeum to identify broader evolutionary conservation and divergence. We identified changes in chromatin architecture and expression dynamics related to desiccation in E. nindensis . It was previously hypothesized that transcriptional re-wiring of seed desiccation pathways confers vegetative desiccation tolerance. We demonstrate that the majority of seed dehydration related genes show similar expression patterns in leaves of desiccation tolerant and sensitive species during dehydration. However, we discovered a small set of orthologs with expression specific to leaves of desiccation tolerant species, and seeds of sensitive species. This supports a nuanced role of seed-related genes where many overlap with typical drought responses but some crucial genes are desiccation specific in resurrection plants.
Desiccation Tolerance
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Recalcitrant seed
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In this master's thesis, the desiccation tolerance of seeds from yeheb, Cordeauxia
edulis Hemsley, a multipurpose, evergreen shrub, native to the semi-desert areas in
the horn of Africa, is studied. Due to overexploitation and bad regeneration, yeheb is
now threatened with extinction.
Seeds of different species can be classified into three storage behaviour categories,
depending on their desiccation tolerance, longevity and tolerance to low temperatures
during storage. When determining the storage behaviour of seeds, the first step is to
study desiccation tolerance. Seeds that maintain their viability at <5% moisture
content (wwb=wet weight basis), are probably orthodox. If they tolerate 10-12.5%
moisture content (MC), but not lower, they may be intermediate, and if most seeds die
when desiccated to moisture contents >15-20%, then they are recalcitrant. Desiccation
tolerance of seeds is controlled by several physiological processes, and depends on
factors such as drying rate, tissue, degree of development at harvest and
environmental influence of the mother plant prior to seed maturation/harvest.
To achieve the desiccation of seeds, silica gel was used. The seeds were dried to six
different moisture contents: 9.6, 12.3, 24.4, 27.4, 33.4 and 39.3% (wwb). Moisture
content of the fresh seeds was 41.6%. Desiccation tolerance was assessed by
germination tests followed by a tetrazolium test of viability on ungerminated seeds
that were not estimated to be clearly dead at the end of the germination test.
Germination tests were done on desiccated and fresh seeds, and on seeds from 'control
of time factor during drying' -replications, in which vermiculite were used instead of
silica gel during the drying treatment. Germination percentage was dependent on seed
moisture content (p-value 0.0001), seen as a reduction of germinability when seed
moisture content dropped from >24.4 to 12.3% (p-value 0.0062). Further drying to
9.6% moisture content, reduced germination percentage even more (70-83.8% at MC
>24.4%, 57.5% at 12.3% MC and 41.3% at 9.6% MC). The reduction of germination
capacity at the latter MC was highly significant compared to the control replications
(p-value 0.0001). Yeheb seeds may therefore be classified as having seeds of
intermediate storage behaviour. However, further studies on viability in storage and
tolerance to low temperatures are necessary before any certain conclusions on the
classification of seed storage behaviour of yeheb can be drawn.
Recalcitrant seed
Desiccation Tolerance
Drought Tolerance
Lenticel
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Desiccation sensitive (DS) seeds do not survive dry storage due to their lack of desiccation tolerance. Almost half of the plant species in tropical rainforests produce DS seeds and therefore the desiccation sensitivity of these seeds represents a problem for and long-term biodiversity conservation. This phenomenon raises questions as to how, where and why DS (desiccation sensitive)-seeded species appeared during evolution. These species evolved probably independently from desiccation tolerant (DT) seeded ancestors. They adapted to environments where the conditions are conducive to immediate germination after shedding, e.g. constant and abundant rainy seasons. These very predictable conditions offered a relaxed selection for desiccation tolerance that eventually got lost in DS seeds. These species are highly dependent on their environment to survive and they are seriously threatened by deforestation and climate change. Understanding of the ecology, evolution and molecular mechanisms associated with seed desiccation tolerance can shed light on the resilience of DS-seeded species and guide conservation efforts. In this review, we survey the available literature for ecological and physiological aspects of DS-seeded species and combine it with recent knowledge obtained from DT model species. This enables us to generate hypotheses concerning the evolution of DS-seeded species and their associated genetic alterations.
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Desiccation Tolerance
Ecophysiology
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A suite of interacting processes and mechanisms enables tolerance of desiccation and storage (conservation) of orthodox seeds in the dry state. While this is a long-term option under optimised conditions, dry orthodox seeds are not immortal, with life spans having been characterised as short, intermediate and long. Factors facilitating desiccation tolerance are metabolic 'switch-off' and intracellular dedifferentiation. Recalcitrant seeds lack these mechanisms, contributing significantly to their desiccation sensitivity. Consequently, recalcitrant seeds, which are shed at high water contents, can be stored only in the short-term, under conditions not allowing dehydration. The periods of such hydrated storage are constrained by germination that occurs without the need for extraneous water, and the proliferation of seed-associated fungi. Cryopreservation is viewed as the only option for long-term conservation of the germplasm of recalcitrant-seeded species. This is not easily achieved, as each of the necessary procedures imposes oxidative damage. Intact recalcitrant seeds cannot be cryopreserved, the common practice being to use excised embryos or embryonic axes as explants. Dehydration is a necessary procedure prior to exposure to cryogenic temperatures, but this is associated with metabolism-linked injury mediated by uncontrolled ROS generation and failing anti-oxidant systems. While the extent to which this occurs can be curtailed by maximising drying rate (flash drying) it cannot be completely obviated. Explant cooling for, and rewarming after, cryostorage must necessarily be rapid, to avoid ice crystallisation. The ramifications of desiccation sensitivity are discussed, as are problems involved in cryostorage, particularly those accompanying dehydration and damage consequent upon ice crystallisation. While desiccation sensitivity is a 'fact' of seed recalcitrance, resolutions of the difficulties involved germplasm conservation are possible as discussed.
Recalcitrant seed
Desiccation Tolerance
Cryptobiosis
Germ plasm
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Desiccation-tolerant (orthodox) seeds can survive in the dry state for considerable periods and so can be stored successfully at low water content and subzero temperatures. Orthodox seeds possess a variety of protective processes and mechanisms that confer desiccation tolerance, important among them being metabolic shutdown and intracellular dedifferentiation. In contrast, desiccation-sensitive (recalcitrant) seeds cannot tolerate water loss and so cannot be stored using conventional seed bank conditions. Particularly with respect to storage, recalcitrant seeds do not undergo intracellular dedifferentiation nor any significant metabolic shutdown. Embryos of recalcitrant seeds remain metabolically active, with little or no reduction in extent of the extensive intracellular membranes. At the water content at which they are shed, with the ongoing metabolism in recalcitrant seeds, developmental phenomena grade imperceptibly into those associated with germination. Thus, recalcitrant seeds can be stored intact only until germination is initiated, which can range from a few days to several months, depending on species. Mild drying to inhibit germination in storage (subimbibed storage) leads to more rapid loss of viability. The only feasible method for long-term storage of germplasm of recalcitrant-seeded species is cryopreservation, but this requires partial drying to prevent ice crystal damage. However, the response to drying depends on the drying rate: slow drying induces viability loss at high water contents, whereas material dried rapidly can survive (in the short term) to water contents low enough to permit vitrification of the remaining intracellular water rather than the formation of ice crystals, if cooling rates are rapid enough. Recalcitrant seeds are almost invariably too large to permit the rates of drying and cooling required for vitrification, and so excised embryonic axes are generally the explants of choice. This review highlights how the physiology of recalcitrant seeds impacts on attempts to cryopreserve the excised embryonic axes/embryos.
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Vitrification
Cryptobiosis
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In the tropics, species with recalcitrant or desiccation-sensitive, Type III seeds are largely restricted to regions with comparatively high rainfall, because desiccation-induced seed death will be minimal in these environments. However, species with recalcitrant seeds do occur in drylands, although little is known about ecological adaptations to minimize seed death in these environments. Here we present data for the seed desiccation tolerance of 10 African dryland species and examine the relationships between seed size, rainfall at the time of seed shed, and desiccation tolerance for these and a further 70 species from the scientific literature. The combined data set encompasses species from 33 families. Three species (Syzygium cumini, Trichilia emetica, and Vitellaria paradoxa) had desiccation-sensitive seeds, and the remaining seven species investigated were desiccation-tolerant. The desiccation-sensitive species had large (>0.5 g) seeds, germinated rapidly, and had comparatively small investments in seed physical defenses. Furthermore, seed was shed in months of high rainfall (>60 mm). In comparison, for species with desiccation-tolerant seeds, seed mass varied across five orders of magnitude, and seed was shed in wet and dry months. Although infrequent in dryland environments (approximately 11% of the species examined here), species with desiccation-sensitive seeds do occur; large size, rapid germination, and the timing of dispersal all reduce the likelihood of seed drying. Furthermore, desiccation-sensitivity may be advantageous for large-seeded species by increasing the efficiency of resource use in seed provisioning.
Desiccation Tolerance
Recalcitrant seed
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SUMMARY The relationship of seed moisture content (fresh weight basis) to germination, and the effect on viability of various storage conditions were examined for five species of the tropical forest tree genus Dipterocarpus. It was shown that seeds fall into two groups with regard to desiccation tolerance. Firstly, D. obtusifolius and D. turbinatus cannot be dried below about 45% moisture content without damage; a sigmoid curve was found to fit the relationship between germination and moisture content for the latter species. Secondly, D. intricatus, D. tuberculatus and D. alatus can be safely dried to 10%, 12% and 17% moisture contents respectively, but desiccation to near 7% moisture content reduced viability by at least a half. Storage studies showed that seed of D. intricatus and D. tuberculatus possessed increased longevity as moisture contents were reduced within the range 6–20%. It was concluded that seeds in the first group are ‘recalcitrant’ and that those in the second group are ‘orthodox’ in their storage physiology, according to the categories described by Roberts (1973). Wide differences between species in seed desiccation rates were observed. In 15% relative humidity D. intricatus dried to 7% moisture content within a week, whilst D. obtusifolius retained 30% moisture content even after 5 wk; other species had intermediate desiccation rates. Seed size and structure may partly account for the differences observed. Correlations were observed between seed storage physiology and other factors which were investigated. ‘Orthodox’ seeds had quicker desiccation rates, were derived from drier habitats, and had smaller embryos than those of ‘recalcitrant’ seeds. ‘Orthodox’ seeds, with the possible exception of D. alatus , should be kept at 0–3°C with about 12% moisture content in the short term and, provided less than 10% germination is lost on freezing, at‐18°C with about 8% moisture content in the long term. ‘Recalcitrant’ seeds should be stored in ventilated containers at 21°C and with moisture contents above 45–50%.
Desiccation Tolerance
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Abstract Development of the highly desiccation-sensitive (recalcitrant) seeds of primarily one species, Avicennia marina , is reviewed and compared with the ontogeny of desiccation-tolerant (orthodox) seeds. A. marina seeds undergo no maturation drying and remain metabolically active throughout development, which grades almost imperceptibly into germination. While PGR control of histodifferentiation is essentially similar to that characterizing desiccation-tolerant seeds, the phase of growth and reserve deposition is characterized by exceedingly high cytokinin levels which, it is proposed, promote a sink for assimilate import. While some starch accumulation does occur, the predominant reserves are soluble sugars which are readily available for the immediate onset of seedling establishment upon shedding. ABA levels are negligible in the embryo tissues during seed maturation, but increase in the pericarp, which imposes a constraint upon germination until these outer coverings are sloughed or otherwise removed. The pattern of proteins synthesized remains qualitatively similar throughout seed development in A. marina , and no LEA proteins are produced. This suggests both that seedling establishment is independent of maturation proteins and that the absence of LEAs and desiccation sensitivity might be causally related. The study on A. marina reveals that for this recalcitrant seed-type, germination per se cannot be defined: rather, it is considered as the continuation of development temporarily constrained by the pericarp ABA levels. This leads to a reexamination of the role of rehydration as key event sensu stricto , in the germination processes in desiccation-tolerant (orthodox) seeds.
Recalcitrant seed
Desiccation Tolerance
Avicennia marina
Avicennia
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