Desiccation tolerance evolved recurrently across diverse plant lineages to enable survival in water-limited conditions. Many resurrection plants are polyploid, and several groups have hypothesized that polyploidy contributed to the evolution of desiccation tolerance. However, due to the vast phylogenetic distance between resurrection plant lineages, the rarity of desiccation tolerance, and the prevalence of polyploidy in plants, this hypothesis has been difficult to test. Here, we surveyed natural variation in morphological, reproductive, and desiccation tolerance traits across several cytotypes of a single species to test for links between polyploidy and increased resilience. We sampled multiple natural populations of the resurrection grass Microchloa caffra across an environmental gradient ranging from mesic to xeric in South Africa. We describe two distinct ecotypes of M. caffra that occupy different extremes of the environmental gradient and exhibit consistent differences in ploidy, morphological, reproductive, and desiccation tolerance traits in both field and common growth conditions. Interestingly, plants with more polyploid genomes exhibited consistently higher recovery from desiccation, were less reproductive, and were larger than plants with smaller genomes and lower ploidy. These data indicate that selective pressures in increasingly xeric sites may play a role in maintaining and increasing desiccation tolerance and are mediated by changes in ploidy.
Two Decades of Desiccation Biology: A Systematic Review of the Best Studied Angiosperm Resurrection Plants
Resurrection plants have an extraordinary ability to survive extreme water loss but still revive full metabolic activity when rehydrated. These plants are useful models to understand the complex biology of vegetative desiccation tolerance. Despite extensive studies of resurrection plants, many details underlying the mechanisms of desiccation tolerance remain unexplored. To summarize the progress in resurrection plant research and identify unexplored questions, we conducted a systematic review of 15 model angiosperm resurrection plants. This systematic review provides an overview of publication trends on resurrection plants, the geographical distribution of species and studies, and the methodology used. Using the Preferred Reporting Items for Systematic reviews and Meta–Analyses protocol we surveyed all publications on resurrection plants from 2000 and 2020. This yielded 185 empirical articles that matched our selection criteria. The most investigated plants were Craterostigma plantagineum (17.5%), Haberlea rhodopensis (13.7%), Xerophyta viscosa (reclassified as X. schlechteri) (11.9%), Myrothamnus flabellifolia (8.5%), and Boea hygrometrica (8.1%), with all other species accounting for less than 8% of publications. The majority of studies have been conducted in South Africa, Bulgaria, Germany, and China, but there are contributions from across the globe. Most studies were led by researchers working within the native range of the focal species, but some international and collaborative studies were also identified. The number of annual publications fluctuated, with a large but temporary increase in 2008. Many studies have employed physiological and transcriptomic methodologies to investigate the leaves of resurrection plants, but there was a paucity of studies on roots and only one metagenomic study was recovered. Based on these findings we suggest that future research focuses on resurrection plant roots and microbiome interactions to explore microbial communities associated with these plants, and their role in vegetative desiccation tolerance.
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- Award ID(s):
- 1906094
- PAR ID:
- 10332280
- Date Published:
- Journal Name:
- Plants
- Volume:
- 10
- Issue:
- 12
- ISSN:
- 2223-7747
- Page Range / eLocation ID:
- 2784
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
Abstract Desiccation-tolerant (DT) organisms can lose nearly all their water without dying. Desiccation tolerance allows organisms to survive in a nearly completely dehydrated, dormant state. At the cellular level, sugars and proteins stabilize cellular components and protect them from oxidative damage. However, there are few studies of the dynamics and drivers of whole-plant recovery in vascular DT plants. In vascular DT plants, whole-plant desiccation recovery (resurrection) depends not only on cellular rehydration, but also on the recovery of organs with unequal access to water. In this study, in situ natural and artificial irrigation experiments revealed the dynamics of desiccation recovery in two DT fern species. Organ-specific irrigation experiments revealed that the entire plant resurrected when water was supplied to roots, but leaf hydration alone (foliar water uptake) was insufficient to rehydrate the stele and roots. In both species, pressure applied to petioles of excised desiccated fronds resurrected distal leaf tissue, while capillarity alone was insufficient to resurrect distal pinnules. Upon rehydration, sucrose levels in the rhizome and stele dropped dramatically as starch levels rose, consistent with the role of accumulated sucrose as a desiccation protectant. These findings provide insight into traits that facilitate desiccation recovery in dryland ferns associated with chaparral vegetation of southern California.more » « less
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SUMMARY Resurrection plants can survive prolonged life without water (anhydrobiosis) in regions with seasonal drying. This desiccation tolerance requires the coordination of numerous cellular processes across space and time, and individual plant tissues face unique constraints related to their function. Here, we analyzed the complex, octoploid genome of the model resurrection plant
Craterostigma (C. plantagineum ), and surveyed spatial and temporal expression dynamics to identify genetic elements underlying desiccation tolerance. Homeologous genes within theCraterostigma genome have divergent expression profiles, suggesting the subgenomes contribute differently to desiccation tolerance traits. TheCraterostigma genome contains almost 200 tandemly duplicated early light‐induced proteins, a hallmark trait of desiccation tolerance, with massive upregulation under water deficit. We identified a core network of desiccation‐responsive genes across all tissues, but observed almost entirely unique expression dynamics in each tissue during recovery. Roots and leaves have differential responses related to light and photoprotection, autophagy and nutrient transport, reflecting their divergent functions. Our findings highlight a universal set of likely ancestral desiccation tolerance mechanisms to protect cellular macromolecules under anhydrobiosis, with secondary adaptations related to tissue function. -
Desiccation tolerance is an ancient and complex trait that spans all major lineages of life on earth. Although important in the evolution of land plants, the mechanisms that underlay this complex trait are poorly understood, especially for vegetative desiccation tolerance (VDT). The lack of suitable closely related plant models that offer a direct contrast between desiccation tolerance and sensitivity has hampered progress. We have assembled high-quality genomes for two closely related grasses, the desiccation-tolerant Sporobolus stapfianus and the desiccation-sensitive Sporobolus pyramidalis . Both species are complex polyploids; S. stapfianus is primarily tetraploid, and S. pyramidalis is primarily hexaploid. S. pyramidalis undergoes a major transcriptome remodeling event during initial exposure to dehydration, while S. stapfianus has a muted early response, with peak remodeling during the transition between 1.5 and 1.0 grams of water (gH 2 O) g −1 dry weight (dw). Functionally, the dehydration transcriptome of S. stapfianus is unrelated to that for S. pyramidalis . A comparative analysis of the transcriptomes of the hydrated controls for each species indicated that S. stapfianus is transcriptionally primed for desiccation. Cross-species comparative analyses indicated that VDT likely evolved from reprogramming of desiccation tolerance mechanisms that evolved in seeds and that the tolerance mechanism of S. stapfianus represents a recent evolution for VDT within the Chloridoideae. Orthogroup analyses of the significantly differentially abundant transcripts reconfirmed our present understanding of the response to dehydration, including the lack of an induction of senescence in resurrection angiosperms. The data also suggest that failure to maintain protein structure during dehydration is likely critical in rendering a plant desiccation sensitive.more » « less
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Many desiccation-tolerant plants are widely distributed and exposed to substantial environmental variation across their native range. These environmental differences generate site-specific selective pressures that could drive natural variation in desiccation tolerance across populations. If identified, such natural variation can be used to target tolerance-enhancing characteristics and identify trait associations within a common genetic background. Here, we tested for natural variation in desiccation tolerance across wild populations of the South African resurrection plant Myrothamnus flabellifolia. We surveyed a suite of functional traits related to desiccation tolerance, leaf economics, and reproductive allocation in M. flabellifolia to test for trait associations and tradeoffs. Despite considerable environmental variation across the study area, M. flabellifolia plants were extremely desiccation tolerant at all sites, suggesting that tolerance is either maintained by selection or fixed in these populations. However, we detected notable associations between environmental variation, population characteristics, and fitness traits. Relative to mesic sites, plants in xeric sites were more abundant and larger, but were slower growing and less reproductive. The negative association between growth and reproduction with plant size and abundance pointed towards a potential growth–abundance tradeoff. The finding that M. flabellifolia is more common in xeric sites despite reductions in growth rate and reproduction suggests that these plants thrive in extreme aridity.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/plants10122784
