1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 71, 2020
  5. Article

Annual Review of Plant Biology

Volume 71, 2020

Desiccation Tolerance: Avoiding Cellular Damage During Drying and Rehydration

Abstract

Desiccation of plants is often lethal but is tolerated by the majority of seeds and by vegetative tissues of only a small number of land plants. Desiccation tolerance is an ancient trait, lost from vegetative tissues following the appearance of tracheids but reappearing in several lineages when selection pressures favored its evolution. Cells of all desiccation-tolerant plants and seeds must possess a core set of mechanisms to protect them from desiccation- and rehydration-induced damage. This review explores how desiccation generates cell damage and how tolerant cells assuage the complex array of mechanical, structural, metabolic, and chemical stresses and survive.Likewise, the stress of rehydration requires appropriate mitigating cellular responses. We also explore what comparative genomics, both structural and responsive, have added to our understanding of cellular protection mechanisms induced by desiccation, and how vegetative desiccation tolerance circumvents destructive, stress-induced cell senescence.

Keyword(s): cellular protection, desiccation, desiccation tolerance, mechanical stress, metabolic stress, reactive oxygen species, resurrection plants, senescence
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-071219-105542
2020-04-29
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-071219-105542.html?itemId=/content/journals/10.1146/annurev-arplant-071219-105542&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adamska I, Roobol‐Bóza M, Lindahl M, Andersson B 1999. Isolation of pigment‐binding early light‐inducible proteins from pea. Eur. J. Biochem. 260:453–60
     [Google Scholar]
  2. 2. 
    Aigner S, Remias D, Karsten U, Holzinger A 2013. Unusual phenolic compounds contribute to ecophysiological performance in the purple-colored green alga Zygogonium ericetorum (Zygnematophyceae, Streptophyta) from a high-alpine habitat. J. Phycol. 49:648–60
     [Google Scholar]
  3. 3. 
    Alamillo JM, Bartels D. 2001. Effects of desiccation on photosynthesis pigments and the ELIP-like dsp 22 protein complexes in the resurrection plant Craterostigma plantagineum. Plant Sci 160:1161–70
     [Google Scholar]
  4. 4. 
    Alamillo JM, Roncarati R, Heino P, Velasco R, Nelson D et al. 1995. Molecular analysis of desiccation tolerance in barley embryos and in the resurrection plant Craterostigma plantagineum. Agronomie 2:161–67
     [Google Scholar]
  5. 5. 
    Alpert P, Oliver MJ. 2002. Drying without dying. Desiccation and Survival in Plants: Drying Without Dying M Black, HW Pritchard 3–43 Wallingford, UK: CABI
     [Google Scholar]
  6. 6. 
    Angelovici R, Galili G, Fernie AR, Fait A 2010. Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15:211–18
     [Google Scholar]
  7. 7. 
    Artur MAS, Costa M-CD, Farrant JM, Hilhorst HWM 2019. Genome-level responses to the environment: plant desiccation tolerance. Emerg. Top. Life Sci. 3:153–63
     [Google Scholar]
  8. 8. 
    Artur MAS, Zhao T, Ligterink W, Schranz E, Hilhorst HWM 2018. Dissecting the genomic diversification of late embryogenesis abundant (LEA) protein gene families in plants. Genome Biol. Evol. 11:459–71
     [Google Scholar]
  9. 9. 
    Asami P, Mundree S, Williams B 2018. Saving for a rainy day: control of energy needs in resurrection plants. Plant Sci 271:62–66
     [Google Scholar]
  10. 10. 
    Asami P, Rupasinghe T, Moghaddam L, Njaci I, Roessner U et al. 2019. Roots of the resurrection plant Tripogon loliiformis survive desiccation without the activation of autophagy pathways by maintaining energy reserves. Front. Plant Sci. 10:459
     [Google Scholar]
  11. 11. 
    Atkinson J, Epand RF, Epand RM 2008. Tocopherols and tocotrienols in membranes: a critical review. Free Radic. Biol. Med. 44:739–64
     [Google Scholar]
  12. 12. 
    Banerjee A, Roychoudhury A. 2016. Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17
     [Google Scholar]
  13. 13. 
    Bartels D, Mattar MZM. 2002. Oropetium thomaeum: a resurrection grass with a diploid genome. Maydica 47:185–92
     [Google Scholar]
  14. 14. 
    Beckett M, Loreto F, Velikova V, Brunetti C, Di Ferdinando M et al. 2012. Photosynthetic limitations and volatile and non-volatile isoprenoids in the poikilochlorophyllous resurrection plant Xerophyta humilis during dehydration and rehydration. Plant Cell Environ 35:2061–74
     [Google Scholar]
  15. 15. 
    Bewley JD. 1979. Physiological aspects of desiccation tolerance. Annu. Rev. Plant Physiol. 30:195–238
     [Google Scholar]
  16. 16. 
    Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H 2012. Seeds: Physiology of Development, Germination and Dormancy New York: SpringerA must-read for all interested in a comprehensive study of seed biology.
  17. 17. 
    Bewley JD, Krochko JE. 1982. Desiccation tolerance. Encyclopedia of Plant Physiology: Physiological Plant Ecology II: Water Relations and Carbon Assimilation OL Lange, PS Nobel, CB Osmond, H Ziegler 325–78 Berlin: Springer
     [Google Scholar]
  18. 18. 
    Bidgare RR, Ondrusek ME, Kennicutt MC, Iturriaga R, Harvey HR 1993. Evidence for a photoprotective function for secondary carotenoids of snow algae. J. Phycol. 29:427–34
     [Google Scholar]
  19. 19. 
    Bilger W, Rimke S, Schreiber U, Lange OL 1989. Inhibition of energy-transfer to photosystem II in lichens by dehydration: different properties of reversibility with green and blue-green phycobionts. J. Plant Physiol. 134:261–68
     [Google Scholar]
  20. 20. 
    Billi D, Potts M. 2002. Life and death of dried prokaryotes. Res. Microbiol. 153:7–12
     [Google Scholar]
  21. 21. 
    Blomstedt C, Griffiths C, Gaff D, Hamill J, Neale A 2018. Plant desiccation tolerance and its regulation in the foliage of resurrection “flowering-plant” species. Agronomy 8:146
     [Google Scholar]
  22. 22. 
    Buitink J, Leprince O. 2004. Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–28
     [Google Scholar]
  23. 23. 
    Challabathula D, Puthur JT, Bartels D 2016. Surviving metabolic arrest: photosynthesis during desiccation and rehydration in resurrection plants. Ann. N. Y. Acad. Sci. 1365:89–99
     [Google Scholar]
  24. 24. 
    Charuvi D, Nevo R, Aviv-Sharon E, Gal A, Kiss V et al. 2019. Chloroplast breakdown during dehydration of a homoiochlorophyllous resurrection plant proceeds via senescence-like processes. Environ. Exp. Bot. 157:100–11
     [Google Scholar]
  25. 25. 
    Chaves MM, Maroco JP, Pereira JS 2003. Understanding plant responses to drought—from genes to the whole plant. Funct. Plant Biol. 30:239–64
     [Google Scholar]
  26. 26. 
    Choi YH, van Spronsen J, Dai Y, Verberne M, Hollmann F et al. 2011. Are natural deep eutectic solvents the missing link in understanding cellular metabolism and physiology. Plant Physiol 156:1701–5
     [Google Scholar]
  27. 27. 
    Costa M-CD, Artur MAS, Maia J, Jonkheer E, Derks MF et al. 2017. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nat. Plants 3:17038
     [Google Scholar]
  28. 28. 
    Costa M-CD, Cooper K, Hilhorst HMW, Farrant JM 2017. Orthodox seeds and resurrection plants: two of a kind. Plant Physiol 175:589–99
     [Google Scholar]
  29. 29. 
    Costa V, Quintanilha A, Moradas‐Ferreira P 2007. Protein oxidation, repair mechanisms and proteolysis in Saccharomyces cerevisiae. IUBMB Life 59:293–98
     [Google Scholar]
  30. 30. 
    Crowe JH, Hoekstra FA, Crowe LM 1992. Anhydrobiosis. Annu. Rev. Physiol. 54:579–99
     [Google Scholar]
  31. 31. 
    Cunningham GL, Burk JH. 1973. The effect of carbonate deposition layers (“Caliche”) on the water status of Larrea divaricata. Am. Midl. Nat 90:474–80
     [Google Scholar]
  32. 32. 
    Dace H, Sherwin HW, Illing N, Farrant JM 1998. Use of metabolic inhibitors to elucidate mechanisms of recovery from desiccation stress in the resurrection plant Xerophyta humilis. Plant Growth Regul 24:171–77
     [Google Scholar]
  33. 33. 
    Dekkers BJW, Costa M-CD, Maia J, Bentsink L, Ligterink W, Hilhorst HWM 2015. Acquisition and loss of desiccation tolerance in seeds: from experimental model to biological relevance. Planta 241:563–77
     [Google Scholar]
  34. 34. 
    Dinakar C, Bartels D. 2012. Light response, oxidative stress management and nucleic acid stability in closely related Linderniaceae species differing in desiccation tolerance. Planta 236:541–55
     [Google Scholar]
  35. 35. 
    Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WGT 2012. The cell walls of green algae: a journey through evolution and diversity. Front. Plant Sci. 3:82
     [Google Scholar]
  36. 36. 
    Fàbregas N, Fernie AR. 2019. The metabolic response to drought. J. Exp. Bot. 70:1077–85
     [Google Scholar]
  37. 37. 
    Farrant JM, Brandt W, Lindsey GG 2007. An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress 1:72–84
     [Google Scholar]
  38. 38. 
    Farrant JM, Cooper K, Dace HJW, Bentley J, Hilgart A 2017. Desiccation tolerance. Plant Stress Physiology S Shabala 217–52 Wallingford, UK: CABI, 2nd ed..
     [Google Scholar]
  39. 39. 
    Farrant JM, Cooper K, Hilgart A, Abdalla KO, Bentley J et al. 2015. A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker). Planta 242:407–26
     [Google Scholar]
  40. 40. 
    Farrant JM, Lehner A, Cooper K, Wiswedel S 2009. Desiccation tolerance in the vegetative tissues of the fern Mohria caffrorum is seasonally regulated. Plant J 57:65–79
     [Google Scholar]
  41. 41. 
    Fernandez-Marin B, Holzinger A, Garcia-Plazola J 2016. Photosynthetic strategies of desiccation-tolerant organisms. Handbook of Photosynthesis M Pessarakli 663–81 Boca Raton, FL: CRC, 3rd ed..
     [Google Scholar]
  42. 42. 
    Gaff DF, Blomstedt C, Neale A, Le T, Hamill J, Ghasempour H 2009. Sporobolus stapfianus, a model desiccation-tolerance grass. Funct. Plant Biol. 36:589–99
     [Google Scholar]
  43. 43. 
    Gaff DF, Churchill DM. 1976. Borya nitida Labill.—an Australian species in the Liliaceae with desiccation-tolerant leaves. Aust. J. Bot. 24:209–24
     [Google Scholar]
  44. 44. 
    Gaff DF, Oliver MJ. 2013. The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct. Plant Biol. 40:315–28
     [Google Scholar]
  45. 45. 
    Gao B, Li X, Zhang D, Liang Y, Yang H et al. 2017. Desiccation tolerance in bryophytes: the dehydration and rehydration transcriptomes in the desiccation-tolerant bryophyte Bryum argenteum. Sci. Rep 7:7571
     [Google Scholar]
  46. 46. 
    Gasulla F, Barreno E, Parages ML, Cámara J, Jiménez C et al. 2016. The role of phospholipase D and MAPK signaling cascades in the adaption of lichen microalgae to desiccation: changes in membrane lipids and phosphoproteome. Plant Cell Physiol 57:1908–20
     [Google Scholar]
  47. 47. 
    Gasulla F, vom Dorp K, Dombrink I, Zähringer U, Gisch N et al. 2013. The role of lipid metabolism in the acquisition of desiccation tolerance in Craterostigma plantagineum: a comparative approach. Plant J 75:726–41
     [Google Scholar]
  48. 48. 
    Gechev TS, Benina M, Obata T, Tohge T, Sujeeth N et al. 2013. Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cell. Mol. Life Sci 70:689–709
     [Google Scholar]
  49. 49. 
    Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D 2012. Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol. Life Sci. 69:3175–86
     [Google Scholar]
  50. 50. 
    Georgieva K, Röding A, Büchel C 2009. Changes in some thylakoid membrane proteins and pigments upon desiccation of the resurrection plant Haberlea rhodopensis. J. Plant Physiol 166:1520–28
     [Google Scholar]
  51. 51. 
    Georgieva K, Sarva E, Keresztes A 2010. Protection of thylakoids against combined light and drought by a luminal substance in the resurrection plant Haberlea rhodopensis. Ann. Bot 105:117–26
     [Google Scholar]
  52. 52. 
    Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48:909–30
     [Google Scholar]
  53. 53. 
    Gusev O, Suetsugu Y, Cornette R, Kawashima T, Logacheva MD et al. 2014. Comparative genome sequencing reveals genomic signature of extreme desiccation tolerance in the anhydrobiotic midge. Nat. Comm. 5:4784–92
     [Google Scholar]
  54. 54. 
    Hanson AD, Henry CS, Fiehn O, de Crécy-Lagard V 2016. Metabolite damage and metabolite damage control in plants. Annu. Rev. Plant Biol. 67:131–52
     [Google Scholar]
  55. 55. 
    Havaux M. 1998. Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–51
     [Google Scholar]
  56. 56. 
    Havaux M, Dall'Osto L, Bassi R 2007. Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–20
     [Google Scholar]
  57. 57. 
    Hilhorst HWM, Farrant JM. 2018. Plant desiccation tolerance: a survival strategy with exceptional prospects for climate-smart agriculture. Annu. Plant Rev. Online 1:2 https://doi.org/10.1002/9781119312994.apr0637
     [Crossref] [Google Scholar]
  58. 58. 
    Hoekstra FA, Golovina EA, Buitink J 2001. Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–38
     [Google Scholar]
  59. 59. 
    Holzinger A, Karsten U. 2013. Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front. Plant Sci. 4:327
     [Google Scholar]
  60. 60. 
    Holzinger A, Pichrtová M. 2016. Abiotic stress tolerance of charophyte green algae: new challenges of omics techniques. Front. Plant Sci. 7:678
     [Google Scholar]
  61. 61. 
    Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Comm. 5:3978
     [Google Scholar]
  62. 62. 
    Hundertmark M, Dimova R, Lengefeld J, Seckler R, Hincha DK 2011. The intrinsically disordered late embryogenesis abundant protein LEA18 from Arabidopsis thaliana modulates membrane stability through binding and folding. Biochim. Biophys. Acta Biomembr. 1808:446–53
     [Google Scholar]
  63. 63. 
    Ingle RA, Collett H, Cooper K, Takahashi Y, Farrant JM, Illing N 2008. Chloroplast biogenesis during rehydration of the resurrection plant Xerophyta humilis: parallels to the etioplast-chloroplast transition. Plant Cell Environ 31:1813–24
     [Google Scholar]
  64. 64. 
    Ingle RA, Schmidt UG, Farrant JM, Thomson JA, Mundree SG 2007. Proteomic analysis of leaf proteins during dehydration of the resurrection plant Xerophyta viscosa. Plant Cell Environ 30:435–46
     [Google Scholar]
  65. 65. 
    Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès J et al. 2009. Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol. Plant. 31:427–36
     [Google Scholar]
  66. 66. 
    Johnson MP, Goral TK, Duffy CD, Brain AP, Mullineaux CW, Ruban AV 2011. Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:1468–79
     [Google Scholar]
  67. 67. 
    Jones RGW, Gorham J. 1983. Osmoregulation. Encyclopedia of Plant Physiology: Physiological Plant Ecology III: Responses to the Chemical and Biological Environment OL Lange, PS Nobel, CB Osmond, H Ziegler 35–58 Berlin: Springer
     [Google Scholar]
  68. 68. 
    Karbaschi MR, Williams B, Taji A, Mundree SG 2016. Tripogon loliiformis elicits a rapid physiological and structural response to dehydration for desiccation tolerance. Funct. Plant Biol. 43:643–55
     [Google Scholar]
  69. 69. 
    Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud P-F et al. 2010. Role of ABA and ABI3 in desiccation tolerance. Science 327:546
     [Google Scholar]
  70. 70. 
    Kobayashi Y, Ando H, Hanaoka M, Tanaka K 2016. Abscisic acid participates in the control of cell cycle initiation through heme homeostasis in the unicellular red alga Cyanidioschyzon merolae. Plant Cell Physiol 57:953–60
     [Google Scholar]
  71. 71. 
    Koster KL, Bryant G. 2006. Dehydration in model membranes and protoplasts: contrasting effects at low, intermediate and high hydrations. Cold Hardiness in Plants THH Chen, M Uemura, S Fujikawa 219–34 Wallingford, UK: CABI
     [Google Scholar]
  72. 72. 
    Kranner I, Beckett R, Hochman A, Nash TH III 2008. Desiccation-tolerance in lichens: a review. Bryologist 111:576–93
     [Google Scholar]
  73. 73. 
    Kranner I, Birtić S, Anderson KM, Pritchard HW 2006. Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death?. Free Rad. Biol. Med. 40:2155–65
     [Google Scholar]
  74. 74. 
    Krasensky J, Jonak C. 2012. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63:1593–608
     [Google Scholar]
  75. 75. 
    Lawlor DW, Tezara W. 2009. Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann. Bot. 103:561–79
     [Google Scholar]
  76. 76. 
    Lee GJ, Pokala N, Vierling E 1995. Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J. Biol. Chem. 270:10432–38
     [Google Scholar]
  77. 77. 
    Leprince O, Pellizzaro A, Berriri S, Buitink J 2017. Late seed maturation: drying without dying. J. Exp. Bot. 68:827–41
     [Google Scholar]
  78. 78. 
    Levitt J. 1980. Water stress. Responses of Plants to Environmental Stresses VII. Water, Radiation, Salt and Other Stresses J Levitt 3–282 New York: Academic
     [Google Scholar]
  79. 79. 
    Liu X, Challabathula D, Quan W, Bartels D 2019. Transcriptional and metabolic changes in the desiccation tolerant plant Craterostigma plantagineum during recurrent exposures to dehydration. Planta 249:1017–35
     [Google Scholar]
  80. 80. 
    Lughadha EN, Govaerts R, Belyaeva I, Black N, Lindon H et al. 2016. Counting counts: revised estimates of numbers of accepted species of flowering plants, seed plants, vascular plants and land plants with a review of other recent estimates. Phytotaxa 272:82–88
     [Google Scholar]
  81. 81. 
    Martinelli T. 2008. In situ localization of glucose and sucrose in dehydrating leaves of Sporobolus stapfianus. J. Plant Physiol 165:580–87
     [Google Scholar]
  82. 82. 
    Mayaba N, Minibayeva F, Beckett RP 2002. An oxidative burst of hydrogen peroxide during rehydration following desiccation in the moss Atrichum androgynum. New Phytol 155:275–83
     [Google Scholar]
  83. 83. 
    Mönke G, Seifert M, Keilwagen J, Mohr M, Grosse I et al. 2012. Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res 40:8240–54
     [Google Scholar]
  84. 84. 
    Montillet JL, Cacas JL, Garnier L, Montane MH, Douki T et al. 2004. The upstream oxylipin profile of Arabidopsis thaliana: a tool to scan for oxidative stresses. Plant J. Cell Mol. Biol. 40:439–51
     [Google Scholar]
  85. 85. 
    Moore JP, Farrant JM. 2012. A systems‐based molecular biology analysis of resurrection plants for crop and forage improvement in arid environments. Improving Crop Resistance to Abiotic Stress N Tuteja, SS Gill, AF Tiburcio, R Tuteja 399–418 Hoboken, NJ: Wiley
     [Google Scholar]
  86. 86. 
    Moore JP, Hearshaw M, Ravenscroft N, Lindsey GG, Farrant JM, Brandt WF 2007. Desiccation-induced ultrastructural and biochemical changes in the leaves of the resurrection plants Myrothamnus flabellifolia. Austr. J. Bot 55:482–91
     [Google Scholar]
  87. 87. 
    Moore JP, Nguema-Ona EE, Vicré-Gibouin M, Sørensen I, Willats WGT et al. 2012. Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237:739–54
     [Google Scholar]
  88. 88. 
    Moore JP, Westall KL, Ravenscroft N, Farrant JM, Lindsey GG, Brandt WF 2005. The predominant polyphenol in the leaves of the resurrection plant Myrothamnnus flabellifolius, 3,4,5 tri-O-galloylquinic acid, protects membranes against desiccation and free radical-induced oxidation. Biochem. J 385:301–8
     [Google Scholar]
  89. 89. 
    Moyankova D, Mladenov P, Berkov S, Peshev D, Georgieva D, Djilianov D 2014. Metabolic profiling of the resurrection plant Haberlea rhodopensis during desiccation and recovery. Physiol. Plant. 152:675–87
     [Google Scholar]
  90. 90. 
    Munné-Bosch S, Alegre L. 2002. The function of tocopherols and tocotrienols in plants. Crit. Rev. Plant Sci. 21:31–57
     [Google Scholar]
  91. 91. 
    Munné-Bosch S, Alegre L. 2004. Die and let live: leaf senescence contributes to plant survival under drought stress. Funct. Plant Biol. 31:203–16
     [Google Scholar]
  92. 92. 
    Nakabayashi K, Okamoto K, Koshiba T, Kamiya Y, Nambara E 2015. Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709
     [Google Scholar]
  93. 93. 
    Navari-Izzo F, Ricci F, Vazzana C, Quartacci MF 1995. Unusual composition of thylakoid membranes of the resurrection plant Boea hygroscopica: changes in lipids upon dehydration and rehydration. Physiol. Plant. 94:135–42
     [Google Scholar]
  94. 94. 
    Oliver MJ, Bewley JD. 1984. Desiccation and ultrastructure in bryophytes. Adv. Bryol. 2:91–131
     [Google Scholar]
  95. 95. 
    Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BWM, Cushman JC 2011. A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23:1231–48
     [Google Scholar]
  96. 96. 
    Oliver MJ, O'Mahony P, Wood AJ 1998. “To dryness and beyond” – preparation for the dried state and rehydration in vegetative desiccation-tolerant plants. Plant Growth Regul 24:193–201
     [Google Scholar]
  97. 97. 
    Oliver MJ, Velten J, Mishler BD 2005. Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats. Integr. Comp. Biol. 45:788–99
     [Google Scholar]
  98. 98. 
    Ooms J, Leon‐Kloosterziel KM, Bartels D, Koornneef M, Karssen CM 1993. Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana (a comparative study using abscisic acid‐insensitive abi3 mutants). Plant Physiol 102:1185–91
     [Google Scholar]
  99. 99. 
    Pardo J, Wai CM, Chay H, Madden CF, Hilhorst HWM et al. 2019. Intertwined signatures of desiccation and drought tolerance in grasses. bioRxiv 662379. https://doi.org/10.1101/662379
    [Crossref]
  100. 100. 
    Parkhey S, Naithani SC, Keshavkant S 2012. ROS production and lipid catabolism in desiccating Shorea robusta seeds during aging. Plant Phys. Biochem. 57:261–67
     [Google Scholar]
  101. 101. 
    Plancot B, Vanier G, Maire F, Bardor M, Lerouge P et al. 2014. Structural characterization of arabinoxylans from two African plant species Eragrostis nindensis and Eragrostis tef using various mass spectrometric methods. Rapid Commun. Mass Spectrom. 28:908–16
     [Google Scholar]
  102. 102. 
    Potts M, Slaughter SM, Hunneke F-U, Garst JF, Helm RF 2005. Desiccation tolerance of prokaryotes: application of principles to human cells. Integr. Comp. Biol. 45:800–9
     [Google Scholar]
  103. 103. 
    Proctor MCF, Oliver MJ, Wood AJ, Alpert P, Stark LR et al. 2007. Desiccation-tolerance in bryophytes: a review. Bryologist 110:595–622A comprehensive look at desiccation tolerance in bryophytes.
     [Google Scholar]
  104. 104. 
    Proctor MCF, Pence VC. 2002. Vegetative tissues: bryophytes, vascular resurrection plants and vegetative propagules. Desiccation and Survival in Plants: Drying Without Dying M Black, HW Pritchard 207–37 Wallingford, UK: CABI
     [Google Scholar]
  105. 105. 
    Quartacci MF, Forli M, Rascio N, Vecchia FD, Bochicchio A, Navari-Izzo F 1997. Desiccation-tolerant Sporobolus stapfianus: lipid composition and cellular ultrastructure during dehydration and rehydration. J. Exp. Bot. 48:1269–79
     [Google Scholar]
  106. 106. 
    Quartacci MF, Glišić O, Stevanović B, Navari‐Izzo F 2002. Plasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydration. J. Exp. Bot. 53:2159–66
     [Google Scholar]
  107. 107. 
    Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69
     [Google Scholar]
  108. 108. 
    Richter K, Haslbeck M, Buchner J 2010. The heat shock response: life on the verge of death. Mol. Cell 40:253–66
     [Google Scholar]
  109. 109. 
    Rizza A, Boccaccini A, Lopez-Vidriero I, Costantino P, Vittorioso P 2011. Inactivation of the ELIP1 and ELIP2 genes affects Arabidopsis seed germination. New Phytol 190:896–905
     [Google Scholar]
  110. 110. 
    Rodriguez MCS, Edsgärd D, Hussain SS, Alquezar D, Rasmussen M et al. 2010. Transcriptomes of the desiccation‐tolerant resurrection plant Craterostigma plantagineum. Plant J 63:212–28
     [Google Scholar]
  111. 111. 
    Ruuska SA, Schwender J, Ohlrogge JB 2004. The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol 136:2700–9
     [Google Scholar]
  112. 112. 
    Sajeev N, Bai B, Bentsink L 2019. Seeds: a unique system to study translational regulation. Trends Plant Sci 24:487–95
     [Google Scholar]
  113. 113. 
    Sgherri C, Stevanovic B, Navari‐Izzo F 2004. Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiol. Plant. 122:478–85
     [Google Scholar]
  114. 114. 
    Sherwin HW, Farrant JM. 1998. Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regul 24:203–10
     [Google Scholar]
  115. 115. 
    Shivaraj YN, Plancot B, Gugi B, Vicré-Gibouin M, Driouich A et al. 2018. Perspectives on structural, physiological, cellular, and molecular responses to desiccation in resurrection plants. Scientifica 2018:9464592An in-depth review of cell wall composition and structural changes associated with desiccation tolerance.
     [Google Scholar]
  116. 116. 
    Shimizu T, Kanamori Y, Furuki T, Kikawada T, Okuda T et al. 2010. Desiccation-induced structuralization and glass formation of group 3 late embryogenesis abundant protein model peptides. Biochemistry 49:1093–104
     [Google Scholar]
  117. 117. 
    Silva AT, Ligterink W, Ribone PA, Chan RL, Hilhorst HWM 2016. A predictive co-expression network identifies novel genes controlling the seed-to-seedling phase transition in Arabidopsis thaliana. Plant Physiol 170:2218–31
     [Google Scholar]
  118. 118. 
    Solhaug KA, Larsson P, Gausla Y 2010. Light screening in lichen cortices can be quantified by chlorophyll fluorescence techniques for both reflecting and absorbing pigments. Planta 231:1003–11
     [Google Scholar]
  119. 119. 
    Stark LR. 2017. Ecology of desiccation tolerance in bryophytes: a conceptual framework and methodology. Bryologist 120:130–66
     [Google Scholar]
  120. 120. 
    Stewart RRC, Bewley JD. 1982. Stability and synthesis of phospholipids during desiccation and rehydration of a desiccation-tolerant and a desiccation-intolerant moss. Plant Physiol 69:724–27
     [Google Scholar]
  121. 121. 
    Suguiyama VF, da Silva EA, Meirelles ST, Centeno DDC, Braga MR 2014. Leaf metabolite profile of the Brazilian resurrection plant Barbacenia purpurea Hook. (Velloziaceae) shows two time-dependent responses during desiccation and recovering. Front. Plant Sci. 5:96
     [Google Scholar]
  122. 122. 
    Sultan SE. 2000. Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–42
     [Google Scholar]
  123. 123. 
    Sun WQ. 2002. Methods for the study of water relations under desiccation stress. Desiccation and Survival in Plants: Drying Without Dying M Black, HW Pritchard 47–92 Wallingford, UK: CABIEssential reading for all embarking on dehydration-based experimentation.
     [Google Scholar]
  124. 124. 
    Takahashi D, Uemura M, Kawamura Y 2018. Freezing tolerance of plant cells: from the aspect of plasma membrane and microdomain. Survival Strategies in Extreme Cold and Desiccation M Iwaya-Inoue, M Sakurai, M Uemura 61–79 Singapore: Springer
     [Google Scholar]
  125. 125. 
    Tardieu F. 2012. Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J. Exp. Bot. 63:25–31
     [Google Scholar]
  126. 126. 
    Tolleter D, Hincha DK, Macherel D 2010. A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. Biochim. Biophys. Acta Biomembr. 1798:1926–33
     [Google Scholar]
  127. 127. 
    Tolleter D, Jaquinod M, Mangavel C, Passirani C, Saulnier P et al. 2007. Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. Plant Cell 19:1580–89
     [Google Scholar]
  128. 128. 
    Tshabuse F, Farrant JM, Humbert L, Moura D, Rainteau D 2018. Glycerolipid analysis during desiccation and recovery of the resurrection plant Xerophyta humilis (Bak) Dur. and Schinz. Plant Cell Environ 41:533–47
     [Google Scholar]
  129. 129. 
    VanBuren R, Pardo J, Wai CM, Evans S, Bartels D 2019. Massive tandem proliferation of ELIPs supports convergent evolution of desiccation tolerance across land plants. Plant Physiol 179:1040–49
     [Google Scholar]
  130. 130. 
    VanBuren R, Wai CM, Pardo J, Giarola V, Ambrosini S et al. 2018. Desiccation tolerance evolved through gene duplication and network rewiring in Lindernia. Plant Cell 30:2943–58
     [Google Scholar]
  131. 131. 
    VanBuren R, Wai CM, Zhang Q, Song X, Edger PP et al. 2017. Seed desiccation mechanisms co‐opted for vegetative desiccation in the resurrection grass Oropetium thomaeum. Plant Cell Environ 40:2292–306
     [Google Scholar]
  132. 132. 
    vander Willigen C, Pammenter NW, Mundree SG, Farrant JM 2001. Some physiological comparisons between the resurrection grass, Eragrostis nindensis, and the related desiccation-sensitive species. Eragrostis curvula. Plant Growth Regul. 35:121–129
     [Google Scholar]
  133. 133. 
    Walters C, Farrant JM, Pammenter NW, Berjak P 2002. Desiccation stress and damage. Desiccation and Survival in Plants: Drying Without Dying M Black, HW Pritchard 207–37 Wallingford, UK: CABI
     [Google Scholar]
  134. 134. 
    Walters C, Koster KL. 2007. Structural dynamics and desiccation damage in plant reproductive organs. Plant Desiccation Tolerance MA Jenks, AJ Wood 251–80 Ames, IA: Blackwell
     [Google Scholar]
  135. 135. 
    Walters C, Pammenter NW, Berjak P, Crane J 2001. Desiccation damage, accelerated ageing and respiration in desiccation tolerant and sensitive seeds. Seed Sci. Res. 11:135–48
     [Google Scholar]
  136. 136. 
    Weissman L, Garty J, Hochman A 2005. Rehydration of the lichen Ramalina lacera results in production of reactive oxygen species and nitric oxide and a decrease in antioxidants. Appl. Environ. Microbiol. 71:2121–29
     [Google Scholar]
  137. 137. 
    Williams B, Njaci I, Moghaddam L, Long H, Dickman MB et al. 2015. Trehalose accumulation triggers autophagy during plant desiccation. PLOS Genet 11:e1005705
     [Google Scholar]
  138. 138. 
    Wood AJ. 2007. The nature and distribution of vegetative desiccation-tolerance in hornworts, liverworts, and mosses. Bryologist 110:163–67
     [Google Scholar]
  139. 139. 
    Xiao L, Yang G, Zhang L, Yang X, Zhao J et al. 2015. The resurrection genome of Boea hygrometrica: a blueprint for survival of dehydration. PNAS 112:5833–37
     [Google Scholar]
  140. 140. 
    Xu Z, Xin T, Bartels D, Li Y, Gu W et al. 2018. Genome analysis of the ancient tracheophyte Selaginella tamariscina reveals evolutionary features relevant to the acquisition of desiccation tolerance. Mol. Plant 11:983–94
     [Google Scholar]
  141. 141. 
    Yobi A, Wone BWM, Xu W, Alexander DC, Guo L et al. 2013. Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. Mol. Plant 6:369–85
     [Google Scholar]
  142. 142. 
    Yobi A, Schlauch KA, Tillet RL, Yim WC, Espinoza C et al. 2017. Sporobolus stapfianus: insights into desiccation tolerance in the resurrection grasses from linking transcriptomics to metabolomics. BMC Plant Biol 17:67
     [Google Scholar]
  143. 143. 
    Yobi A, Wone BWM, Xu W, Alexander DC, Guo L et al. 2012. Comparative metabolic profiling between desiccation‐sensitive and desiccation‐tolerant species of Selaginella reveals insights into the resurrection trait. Plant J 72:983–99
     [Google Scholar]
  144. 144. 
    Zeng Q, Chen X, Wood AJ 2002. Two early light‐inducible protein (ELIP) cDNAs from the resurrection plant Tortula ruralis are differentially expressed in response to desiccation, rehydration, salinity, and high light. J. Exp. Bot. 53:1197–205
     [Google Scholar]
  145. 145. 
    Zhang J, Zhang W-M, Downing A, Wu N, Zhang BC 2016. Photosynthetic and cytological recovery on remoistening Syntrichia caninervis Mitt., a desiccation-tolerant moss from Northwestern China. Photosynthetica 49:13–20
     [Google Scholar]
  146. 146. 
    Zhang Q, Bartels D. 2018. Molecular responses to dehydration and desiccation in desiccation-tolerant angiosperm plants. J. Exp. Bot. 69:3211–22
     [Google Scholar]
  147. 147. 
    Zhang Q, Song X, Bartels D 2016. Enzymes and metabolites in carbohydrate metabolism of desiccation tolerant plants. Proteomes 4:40
     [Google Scholar]
  148. 148. 
    Zhu Y, Wang B, Phillips J, Zhang ZN, Du H et al. 2015. Global transcriptome analysis reveals acclimation-primed processes involved in the acquisition of desiccation tolerance in Boea hygrometrica. Plant Cell Physiol 56:1429–41
     [Google Scholar]
  149. 149. 
    Zia A, Walker BJ, Oung HMO, Chavuri D, Jahns P et al. 2016. Protection of the photosynthetic apparatus against dehydration stress in the resurrection plant Craterostigma pumilum. Plant J 87:664–80
     [Google Scholar]
  150. 150. 
    Zinsmeister J, Lalanne D, Terrasson E, Chatelain E, Vandecasteele C et al. 2016. ABI5 is a regulator of seed maturation and longevity in legumes. Plant Cell 28:2735–54
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-071219-105542
Loading
Desiccation Tolerance: Avoiding Cellular Damage During Drying and Rehydration
Annual Review of Plant Biology 71, 435 (2020); https://doi.org/10.1146/annurev-arplant-071219-105542
/content/journals/10.1146/annurev-arplant-071219-105542
/content/journals/10.1146/annurev-arplant-071219-105542
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error