Exploring the mechanisms of desert plant adaptation to arid climates: a multi-omics analysis of dehydration and rehydration responses in Syntrichia caninervis

Abstract

Desert plants have evolved remarkable adaptations to survive in arid environments, where water scarcity and extreme temperatures pose significant challenges to life. The desert moss Syntrichia caninervis stands out as an exemplary model of extreme desiccation tolerance (DT), offering invaluable insights into plant adaptation to water deficit. This study presents a comprehensive multi-omics analysis of S. caninervis during controlled dehydration and rehydration process, integrating transcriptomic, proteomic, and metabolomic data to elucidate the molecular mechanisms underlying its remarkable resilience. Our findings reveal a sophisticated, multilayered response characterized by extensive transcriptional reprogramming (3,153 differentially expressed genes), dynamic proteome remodeling (873 differentially expressed proteins), and strategic metabolic reconfiguration (185 differentially abundant metabolites). Key adaptations include the coordinated downregulation of photosynthetic processes, upregulation of stress-responsive genes and proteins, accumulation of protective metabolites, and enhancement of antioxidant systems. Notably, we observed significant temporal asynchrony between transcript and protein levels, underscoring the complexity of post-transcriptional regulation in stress responses. The core mechanisms of S. caninervis DT comprises cellular protection and metabolic dormancy during dehydration, followed by efficient repair and recovery processes upon rehydration. These findings not only advance our understanding of plant evolution and adaptation to extreme environments but also identify potential targets for enhancing drought tolerance in crops and exploring plant survival under extreme environment. By deciphering the molecular basis of extreme DT, this research opens new avenues for addressing agricultural challenges in water-limited environments and expands our knowledge of plant life's adaptability to harsh terrestrial.

Keywords

Desert moss / Desiccation tolerance / Extremophile adaptation / Extreme environment / Multi-omics integration

References

[1] Becker J, Craig EA. Heat-shock proteins as molecular chaperones. Eur J Biochem, 1994, 219: 11-23

[2] Bruce TJ, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608. https://doi.org/10.1016/j.plantsci.2007.09.002

[3] Chaffai R, Ganesan M, Cherif A (2024) Transcriptional Regulation of Gene Expression in Plant Abiotic Stress Response. In: Plant Adaptation to Abiotic Stress: From Signaling Pathways and Microbiomes to Molecular Mechanisms. Springer, Singapore pp:303–343. https://doi.org/10.1007/978-981-97-0672-3_13

[4] Challabathula D, Zhang Q, Bartels D. Protection of photosynthesis in desiccation-tolerant resurrection plants. J Plant Physiol, 2018, 227: 84-92

[5] Chen P, Jung NU, Giarola V, Bartels D. The dynamic responses of cell walls in resurrection plants during dehydration and rehydration. Front Plant Sci, 2020, 10: 1698

[6] Coe KK, Greenwood JL, Slate ML, Clark TA, Brinda JC, Fisher KM, Mishler BD, Bowker MA, Oliver MJ, Ebrahimi S, Stark LR. Strategies of desiccation tolerance vary across life phases in the moss Syntrichia caninervis. Am J Bot, 2021, 108: 249-262

[7] Costa MCD, Artur MA, Maia J, Jonkheer E, Derks MF, Nijveen H, Williams B, Mundree MD, Jimenez-Gomez JM, Hesselink T, Schijlen EGWM, Ligterink W, Oliver MJ, Farrant JM, Hilhorst HWM. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nat Plants, 2017, 3: 1-10

[8] Dinakar C, Bartels D. Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis. Front Plant Sci, 2013, 4: 482

[9] Ding Y, Fromm M, Avramova Z. Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat Commun, 2012, 3: 740

[10] Elbert W, Weber B, Burrows S, Steinkamp J, Budel B, Andreae MO, Poschl U. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci, 2012, 5: 459-462

[11] ElSayed AI, Rafudeen MS, Golldack D. Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol, 2014, 16: 1-8

[12] Farrant JM, Hilhorst HWM. What is dry? Exploring metabolism and molecular mobility at extremely low water contents. J Exp Bot, 2021, 72: 1507-1510

[13] Farrant JM, Cooper K, Hilgart A, Abdalla KO, Bentley J, Thomson JA, Dace HJW, Peton N, Mundree SG, Rafudeen MS. A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker). Planta, 2015, 242: 407-426

[14] Gao B, Zhang D, Li X, Yang H, Zhang Y, Wood AJ. De novo transcriptome characterization and gene expression profiling of the desiccation tolerant moss Bryum argenteum following rehydration. BMC Genomics, 2015, 16: 1-14

[15] Gao B, Li X, Liang Y, Chen M, Liu H, Liu Y, Wang J, Zhang J, Zhang Y, Oliver MJ, Zhang D. Drying without dying: A genome database for desiccation-tolerant plants and evolution of desiccation tolerance. Plant Physiol, 2024, 194: 2249-2262

[16] Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D. Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol Life Sci, 2012, 69: 3175-3186

[17] Giarola V, Hou Q, Bartels D. Angiosperm plant desiccation tolerance: hints from transcriptomics and genome sequencing. Trends Plant Sci, 2017, 22: 705-717

[18] Goyal P, Devi R, Verma B, Hussain S, Arora P, Tabassum R, Gupta S. WRKY transcription factors: Evolution, regulation, and functional diversity in plants. Protoplasma, 2023, 260: 331-348

[19] Hoekstra FA, Golovina EA, Buitink J. Mechanisms of plant desiccation tolerance. Trends Plant Sci, 2001, 6: 431-438

[20] Huang J, Li Y, Fu C, Chen F, Fu Q, Dai A, Shinoda M, Ma Z, Guo W, Li Z, Zhang L, Liu Y, Yu H, He Y, Xie Y, Guan X, Ji M, Lin L, Wang S, Yan H, Wang G. Dryland climate change: Recent progress and challenges. Rev Geophys, 2017, 55: 719-778

[21] Kappel C, Friedrich T, Oberkofler V, Jiang L, Crawford T, Lenhard M, Bäurle I. Genomic and epigenomic determinants of heat stress-induced transcriptional memory in Arabidopsis. Genome Biol, 2023, 24: 129

[22] Li X, Bai W, Yang Q, Yin B, Zhang Z, Zhao B, Kuang T, Zhang Y, Dao Z. The extremotolerant desert moss Syntrichia caninervis is a promising pioneer plant for colonizing extraterrestrial environments. The Innovation, 2024, 5 100689

[23] Liu J, Moyankova D, Djilianov D, Deng X. Common and specific mechanisms of desiccation tolerance in two Gesneriaceae resurrection plants. Multiomics Evidences. Front Plant Sci, 2019, 10: 1067

[24] Liu X, Zhou P, Li X, Zhang D. Propagation of desert moss Syntrichia caninervis in peat pellet: a method for rapidly obtaining large numbers of cloned gametophytes. Plant Methods, 2021, 17: 1-10

[25] Ma Z, Hu L, Jiang W. Understanding AP2/ERF transcription factor responses and tolerance to various abiotic stresses in plants: A comprehensive review. Int J Mol Sci, 2024, 25: 893

[26] Marks RA, Van L, Schuster J, Gilman IS, VanBuren R (2024) Convergent evolution of desiccation tolerance in grasses. Nat Plants 10:1112–1125. https://doi.org/10.1038/s41477-024-01729-5

[27] Mohanta TK, Mohanta YK, Kaushik P, Kumar J. Physiology, genomics, and evolutionary aspects of desert plants. J Adv Res, 2024, 58: 63-78

[28] Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM (2009) Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci 14:110–117. https:// https://doi.org/10.1016/j.tplants.2008.11.007

[29] Nie S, Wang D. AP2/ERF transcription factors for tolerance to both biotic and abiotic stress factors in plants. Trop Plant Biol, 2023, 16: 105-112

[30] Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BW, Cushman JC. A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell, 2011, 23: 1231-1248

[31] Oliver MJ, Farrant JM, Hilhorst HW, Mundree S, Williams B, Bewley JD. Desiccation tolerance: avoiding cellular damage during drying and rehydration. Annu Rev Plant Biol, 2020, 71: 435-460

[32] Pan Z, Pitt WG, Zhang Y, Wu N, Tao Y, Truscott TT. The upside-down water collection system of Syntrichia caninervis. Nat Plants, 2016, 2: 1-5

[33] Pan Y, Lin W (2024) Moss surviving Mars-like extreme conditions. Innovation 5(5):100689. https://doi.org/10.1016/j.xinn.2024.100689

[34] Pravalie R. Drylands extent and environmental issues. A Global Approach. Earth-Sci Rev, 2016, 161: 259-278

[35] Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 33(3):290–295. https://doi.org/10.1038/nbt.3122

[36] Rathnayake KN, Nelson S, Seeve C, Oliver MJ, Koster KL. Acclimation and endogenous abscisic acid in the moss Physcomitrella patens during acquisition of desiccation tolerance. Physiol Plant, 2019, 167: 317-329

[37] Rodriguez-Caballero E, Belnap J, Budel B, Crutzen PJ, Andreae MO, Poschl U, Weber B. Dryland photoautotrophic soil surface communities endangered by global change. Nat Geosci, 2018, 11: 185-189

[38] Silva AT, Gao B, Fisher KM, Mishler BD, Ekwealor JTB, Stark LR, Li X, Zhang D, Bowker MA, Brinda JC, Coe KK, Oliver MJ. To dry perchance to live: Insights from the genome of the desiccation-tolerant biocrust moss Syntrichia caninervis. Plant J, 2021, 105: 1339-1356

[39] Song H, Cao Y, Zhao L, Zhang J, Li S. WRKY transcription factors: Understanding the functional divergence. Plant Sci, 2023, 334 111770

[40] Stark LR, Nichols LII, McLetchie DN, Bonine ML. Do the sexes of the desert moss Syntrichia caninervis differ in desiccation tolerance? A leaf regeneration assay. Int J Plant Sci, 2005, 166: 21-29

[41] Stark LR, McLetchie DN, Roberts SP. Gender differences and a new adult eukaryotic record for upper thermal tolerance in the desert moss Syntrichia caninervis. J Therm Biol, 2009, 34: 131-137

[42] Sun RZ, Liu J, Wang YY, Deng X (2021) DNA methylation-mediated modulation of rapid desiccation tolerance acquisition and dehydration stress memory in the resurrection plant Boea hygrometrica. PLoS Genet 17(4). https://doi.org/10.1371/journal.pgen.1009549

[43] Vidovic M, Battisti I, Pantelic A, Morina F, Arrigoni G, Masi A, Jovanovic SV (2022) Desiccation tolerance in Ramonda Serbica panc.: an integrative transcriptomic, proteomic, metabolite and photosynthetic study. Plants 11:1199. https://doi.org/10.3390/plants11091199

[44] Wehmeyer N, Vierling E. The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol, 2000, 122: 1099-1108

[45] Xu X, Legay S, Sergeant K, Zorzan S, Leclercq CC, Charton S, Giarola V, Liu X, Challabathula D, Renaut J, Hausman JF, Bartels D, Guerriero G. Molecular insights into plant desiccation tolerance: Transcriptomics, proteomics and targeted metabolite profiling in Craterostigma plantagineum. Plant J, 2021, 107: 377-398

[46] Yang Q, Yang R, Gao B, Liang Y, Liu X, Li X, Zhang D. Metabolomic Analysis of the Desert Moss Syntrichia caninervis Provides Insights into Plant Dehydration and Rehydration Response. Plant Cell Physiol, 2023, 64: 1419-1432

[47] Yang R, Li X, Yang Q, Zhao M, Bai W, Liang Y, Liu X, Gao B, Zhang D. Transcriptional profiling analysis providing insights into desiccation tolerance mechanisms of the desert moss Syntrichia caninervis. Front Plant Sci, 2023, 14: 1127541

[48] Yobi A, Wone BW, Xu W, Alexander DC, Guo L, Ryals JA, Oliver MJ, Cushman JC. Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. Mol Plant, 2013, 6: 369-385

[49] Zhang Y. The microstructure and formation of biological soil crusts in their early developmental stage. Chin Sci Bull, 2005, 50: 117-121

[50] Zhang J, Zhang Y. Ecophysiological responses of the biocrust moss Syntrichia caninervis to experimental snow cover manipulations in a temperate desert of central Asia. Ecol Res, 2020, 35: 198-207

[51] Zhang Y, Wang H, Wang X, Yang W, Zhang D. The microstructure of microbiotic crust and its influence on wind erosion for a sandy soil surface in the Gurbantunggut Desert of Northwestern China. Geoderma, 2006, 132: 441-449

[52] Zhang J, Zhang YM, Downing A, Wu N, Zhang BC. Photosynthetic and cytological recovery on remoistening Syntrichia caninervis mitt., a desiccation-tolerant moss from northwestern China. Photosynthetica, 2011, 49: 13-20

[53] Zhang Z, Wang B, Sun D, Deng X. Molecular cloning and differential expression of sHSP gene family members from the resurrection plant Boea hygrometrica in response to abiotic stresses. Biologia, 2013, 68: 651-661

[54] Zuo DD, Ahammed GJ, Guo DL (2023) Plant transcriptional memory and associated mechanism of abiotic stress tolerance. Plant Physiol Biochem 107917. https://doi.org/10.1016/j.plaphy.2023.107917

Funding

Natural Science Foundation of Xinjiang Uygur Autonomous Region(Grant No. 2022D01E96)

Stable Support for Youth Teams in Basic Research Field of the Chinese Academy of Sciences(YSBR-119)

Leading Talents in Technological Innovation program(2022TSYCLJ0049)

Third Xinjiang Scientific Expedition Program(Grant No.2021xjkk0500)

RIGHTS & PERMISSIONS

The Author(s)