The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon
Donald F. Gaff A C and Melvin Oliver BA School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.
B USDA-ARS, Plant Genetics Research Unit, 205 Curtis Hall – UMC, Columbia, MO 65211, USA.
C Corresponding author. Email: don.gaff@monash.edu
Functional Plant Biology 40(4) 315-328 https://doi.org/10.1071/FP12321
Submitted: 28 October 2012 Accepted: 10 January 2013 Published: 22 February 2013
Abstract
In a minute proportion of angiosperm species, rehydrating foliage can revive from airdryness or even from equilibration with air of ~0% RH. Such desiccation tolerance is known from vegetative cells of some species of algae and of major groups close to the evolutionary path of the angiosperms. It is also found in the reproductive structures of some algae, moss spores and probably the aerial spores of other terrestrial cryptogamic taxa. The occurrence of desiccation tolerance in the seed plants is overwhelmingly in the aerial reproductive structures; the pollen and seed embryos. Spatially and temporally, pollen and embryos are close ontogenetic derivatives of the angiosperm microspores and megaspores respectively. This suggests that the desiccation tolerance of pollen and embryos derives from the desiccation tolerance of the spores of antecedent taxa and that the basic pollen/embryo mechanism of desiccation tolerance has eventually become expressed also in the vegetative tissue of certain angiosperm species whose drought avoidance is inadequate in micro-habitats that suffer extremely xeric episodes. The protective compounds and processes that contribute to desiccation tolerance in angiosperms are found in the modern groups related to the evolutionary path leading to the angiosperms and are also present in the algae and in the cyanobacteria. The mechanism of desiccation tolerance in the angiosperms thus appears to have its origins in algal ancestors and possibly in the endosymbiotic cyanobacteria-related progenitor of chloroplasts and the bacteria-related progenitor of mitochondria. The mechanism may involve the regulation and timing of the accumulation of protective compounds and of other contributing substances and processes.
Additional keywords: abscisic acid, Borya, Craterostigma, gene expression, modular evolution, proteome, protoplasmic drought tolerance, Sporobolus, Tortula, Xerophyta.
References
Abd El-Baky H, El Baz F, El-Baroty G (2009) Enhancement of antioxidant production in Spirulina platensis under oxidative stress. Acta Physiologiae Plantarum 31, 623–631.| Enhancement of antioxidant production in Spirulina platensis under oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Abel WO (1956) Die Austrocknungsresistenz der Laubmose. Sitzungberichte der Wien Akademie der Wissenschaften, Mathematisch-naturwissenschaftliche Klasse, Abteilung I 165, 619–707.
Alamillo J, Almoguera C, Bartels D, Jordano J (1995) Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Molecular Biology 29, 1093–1099.
| Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar |
Antipov N, Romanyak A (1983) Poikilohydric vegetative organs of reproduction in some flowering plants. Zhurnal Obshchei Biologii 44, 446–450. [In Russian]
Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integrative and Comparative Biology 45, 696–701.
| Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar |
Bartels D, Schneider K, Terstappen G, Piatowski D, Salamini F (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181, 27–34.
| Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar |
Bartels D, Hancke C, Schneider K, Michel D, Salamini F (1992) A desiccation-related ELIP-like protein from the resurrection plant Craterostigma plantagineum is regulated by light and ABA. EMBO Journal 11, 2771–2778.
Bartels D, Phillips J, Chandler J (2007) Desiccation tolerance: gene expression, pathways, and regulation of gene expression. In ‘Plant desiccation tolerance’. (Eds M Jenk, AJ Wood) pp. 115–150. (Blackwell Publishing: Ames, IA)
Bewley JD (1979) Physiological aspects of desiccation tolerance. Annual Review of Plant Physiology 30, 195–238.
| Physiological aspects of desiccation tolerance.Crossref | GoogleScholarGoogle Scholar |
Bewley JD, Oliver MJ (1992) Desiccation-tolerance in vegetative plant tissues and seeds: protein synthesis in relation to desiccation and a potential role for protection and repair mechanisms. In ‘Water and life: a comparative analysis of water relationships at the organismic, cellular and molecular levels’. (Eds CB Osmond, G Somero) pp. 141–160. (Springer-Verlag: Berlin)
Blomstedt CK, Griffiths CA, Fredericks DP, Hamill JD, Gaff DF, Neale AD (2010) The resurrection plant Sporobolus stapfianus; an unlikely model for engineering enhance plant biomass. Plant Growth Regulation 62, 217–232.
| The resurrection plant Sporobolus stapfianus; an unlikely model for engineering enhance plant biomass.Crossref | GoogleScholarGoogle Scholar |
Browne J, Tunnacliffe A, Burnell A (2002) Plant desiccation gene found in a nematode. Nature 416, 38
| Plant desiccation gene found in a nematode.Crossref | GoogleScholarGoogle Scholar |
Buitink J, Leger JJ, Guisle I, Vu BL, Wuillème S, Lamirault G, Le Bars A, Le Meur N, Becker A, Küster H, Leprince O (2006) Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago truncatula seeds. The Plant Journal 47, 735–750.
| Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago truncatula seeds.Crossref | GoogleScholarGoogle Scholar |
Clausen E (1952) Hepatics and humidity. Dansk Botansk Archiv 15, 1–80.
Collén J, Hervé C, Guisele-Marsollier I, Léger JL, Boyen C (2006) Expression profiling of Chondrus crispus (Rhodophyta) after exposure to methyl jasmonate. Journal of Experimental Botany 57, 3869–3881.
| Expression profiling of Chondrus crispus (Rhodophyta) after exposure to methyl jasmonate.Crossref | GoogleScholarGoogle Scholar |
Collett H, Shen A, Gardner M, Farrant JM, Denby KJ, Illing N (2004) Toward transcript profiling of desiccation tolerance in Xerophyta humilis: construction of a normalized 11 k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration. Physiologia Plantarum 122, 39–53.
| Toward transcript profiling of desiccation tolerance in Xerophyta humilis: construction of a normalized 11 k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration.Crossref | GoogleScholarGoogle Scholar |
Cruz de Carvalho R, Cartalá M, Marques da Silva J, Branquinho C, Barreno E (2012) The impact of dehyration rate on the production and cellular location of reactive oxygen species in an aquatic moss. Annals of Botany 110, 1007–1016.
| The impact of dehyration rate on the production and cellular location of reactive oxygen species in an aquatic moss.Crossref | GoogleScholarGoogle Scholar |
Cushman JC, Oliver MJ (2011) Understanding vegetative desiccation tolerance using integrated functional genomics approaches within a comparative evolutionary framework. In ‘Plant desiccation tolerance’. (Eds U Lüttge, E Beck, D Bartels) pp. 307–338. (Springer: Heidelberg)
Daniel V, Gaff DF (1980) Desiccation-induced changes in the protein complement of soluble extracts from leaves of resurrection plants and related desiccation-sensitive species. Annals of Botany 45, 174–181.
Danielson JA, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BioMed Central Plant Biology 8, 45
Davis JS (1972) Survival records in the algae, and the survival role of certain algal pigments, fats and mucilaginous substances. Biologist 54, 52–93.
De Saussure T (1827) De l’influence du dessèchement sur la germination de plusieurs grains alimentaires. Annales des Sciences Naturelles 10, 68–93.
Dinakar C, Djilianovb D, Bartels D (2012) Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Science 182, 29–41.
| Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense.Crossref | GoogleScholarGoogle Scholar |
Dinter K (1919) Pflanzenarten aus Deutsch-suedwestafrika. XLIII. Feddes Repertorium 16, 239–244.
| Pflanzenarten aus Deutsch-suedwestafrika. XLIII.Crossref | GoogleScholarGoogle Scholar |
Dixon K, Kuo J, Pate J (1983) Storage reserves of the seed-like, aestivating organs of geophytes inhabiting granite outcrops in south-western Australia. Australian Journal of Botany 31, 85–103.
| Storage reserves of the seed-like, aestivating organs of geophytes inhabiting granite outcrops in south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Farrant JM (2007) Mechanisms of desiccation tolerance in angiosperm resurrection plants. In ‘Plant desiccation tolerance.’ (Eds MA Jenks, AJ Wood) pp. 51–90. (Blackwell Publishing: Ames, IA)
Farrant J, Kruger L (2001) Longevity of dry Myrothamnus flabellifolius in simulated field conditions. Plant Growth Regulation 35, 109–120.
| Longevity of dry Myrothamnus flabellifolius in simulated field conditions.Crossref | GoogleScholarGoogle Scholar |
Farrant J, Moore J (2011) Programming desiccation-tolerance: from plants to seeds to resurrection plants. Current Opinion in Plant Biology 14, 340–345.
| Programming desiccation-tolerance: from plants to seeds to resurrection plants.Crossref | GoogleScholarGoogle Scholar |
Forster PI, Thompson EJ (1997) Borya inopinata (Anthericaceae), a new species of resurrection plant from north Queensland. Austrobaileya 4, 597–600.
Gaff D (1972) Drought resistance of Welwitschia mirabilis Hook. fil. Dinteria 7, 3–8.
Gaff DF (1977) Desiccation tolerant vascular plants of southern Africa. Oecologia 31, 95–109.
| Desiccation tolerant vascular plants of southern Africa.Crossref | GoogleScholarGoogle Scholar |
Gaff DF (1980) Protoplasmic tolerance of extreme water stress. In ‘Adaptation of plants to water and high temperature stress’. (Eds NC Turner, PJ Kramer) pp. 207–230. (John Wiley & Sons: New York)
Gaff DF (1981) The biology of resurrection plants. In ‘The biology of Australian plants’. (Eds JS Pate, AJ McComb) pp. 114–146. (University of Western Australia Press: Nedlands, WA)
Gaff DF (1987) Desiccation tolerant plants in South America. Oecologia 74, 133–136.
| Desiccation tolerant plants in South America.Crossref | GoogleScholarGoogle Scholar |
Gaff DF, Churchill DM (1976) Borya nitida Labill. — an Australian species in the Liliaceae with desiccation-tolerant leaves. Australian Journal of Botany 24, 209–224.
| Borya nitida Labill. — an Australian species in the Liliaceae with desiccation-tolerant leaves.Crossref | GoogleScholarGoogle Scholar |
Gaff DF, Giess W (1986) Drought resistance in water plants in rock pools in southern Africa. Dinteria 18, 17–36.
Gaff DF, Hallam ND (1974) Resurrecting desiccated plants. Royal Society of New Zealand Bulletin 12, 389–393.
Gaff DF, Latz PK (1978) The occurrence of resurrection plants in the Australian flora. Australian Journal of Botany 26, 485–492.
| The occurrence of resurrection plants in the Australian flora.Crossref | GoogleScholarGoogle Scholar |
Gaff DF, Loveys BR (1984) Abscisic acid content and effects during dehydration of detached leaves of desiccation tolerant plants. Journal of Experimental Botany 35, 1350–1358.
| Abscisic acid content and effects during dehydration of detached leaves of desiccation tolerant plants.Crossref | GoogleScholarGoogle Scholar |
Gaff DF, Loveys BR (1993) Abscisic acid levels in drying plants of a resurrection grass. Transactions of the Malaysian Society of Plant Physiology 3, 286–287.
Gaff D, Ziegler H (1989) ATP and ADP contents in leaves of drying and rehydrating desiccation-tolerant plants. Oecologia 78, 407–410.
| ATP and ADP contents in leaves of drying and rehydrating desiccation-tolerant plants.Crossref | GoogleScholarGoogle Scholar |
Gaff D, Blomstedt C, Neale A, Le T, Hamill J, Ghasempour H (2009) Sporobolus stapfianus, a model desiccation-tolerant grass. Functional Plant Biology 36, 589–599.
| Sporobolus stapfianus, a model desiccation-tolerant grass.Crossref | GoogleScholarGoogle Scholar |
Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D (2012) Molecular mechanisms of desiccation tolerance in resurrection plants. Cellular and Molecular Life Sciences: CMLS 69, 3175–3186.
| Molecular mechanisms of desiccation tolerance in resurrection plants.Crossref | GoogleScholarGoogle Scholar |
Gechev TS, Benina M, Obata T, Tohge T, Sujeeth N, Minkov I, Hille J, Temanni M-R, Marriot AS, Bergström E, Thomas-Oates J, Antonio C, Mueller-Roeber B, Schippers JHM, Fernie AR, Toneva V (2013) Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cellular and Molecular Life Sciences 70, 689–704.
| Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis.Crossref | GoogleScholarGoogle Scholar |
Ghasempour H, Anderson E, Gianello RD, Gaff D (1998) Growth inhibitor effects on the protoplasmic drought tolerance and protein synthesis in the leaf cells of the resurrection grass Sporobolus stapfianus. Plant Growth Regulation 24, 179–183.
| Growth inhibitor effects on the protoplasmic drought tolerance and protein synthesis in the leaf cells of the resurrection grass Sporobolus stapfianus.Crossref | GoogleScholarGoogle Scholar |
Ghasempour HR, Gaff DF, Williams RP, Gianello RD (1998b) Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regulation 24, 185–191.
| Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses.Crossref | GoogleScholarGoogle Scholar |
Ghasempour H, Anderson E, Gaff D (2001) Effects of growth substances on the protoplasmic drought tolerance of leaf cells of the resurrection grass Sporobolus stapfianus. Australian Journal of Plant Physiology 28, 1115–1120.
Gould S, Waller R, McFadden G (2008) Plastid evolution. Annual Review of Plant Biology 59, 491–517.
| Plastid evolution.Crossref | GoogleScholarGoogle Scholar |
Goyal K, Walton L, Browne J, Burnell A, Tunnacliffe A (2005a) Molecular anhydrobiology: identifying molecules implicated in invertebrate anhydrobiosis. Integrative and Comparative Biology 45, 702–709.
| Molecular anhydrobiology: identifying molecules implicated in invertebrate anhydrobiosis.Crossref | GoogleScholarGoogle Scholar |
Goyal K, Walton L, Tunnacliffe A (2005b) LEA proteins prevent protein aggregation due to water stress. The Biochemical Journal 388, 151–157.
| LEA proteins prevent protein aggregation due to water stress.Crossref | GoogleScholarGoogle Scholar |
Grant B, Howard R, Gayler K (1976) Isolation and properties of chloroplasts from the siphonous green alga Caulerpa simpliciuscula. Australian Journal of Plant Physiology 3, 639–651.
Halda J (1979) A new intergeneric hybrid in the family Gesneraceae. Preslia, Praha 51, 375–376.
Hartung W (2010) The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Functional Plant Biology 37, 806–812.
| The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen.Crossref | GoogleScholarGoogle Scholar |
Hartung W, Weiler EW, Volk OH (1987) Immunological evidence that abscisic acid is produced by several species of Anthocerotae and Marchantiales. The Bryologist 90, 393–400.
| Immunological evidence that abscisic acid is produced by several species of Anthocerotae and Marchantiales.Crossref | GoogleScholarGoogle Scholar |
Heddad M, Adamska I (2002) The evolution of light stress proteins in photosynthetic organisms. Comparative and Functional Genomics 3, 504–510.
| The evolution of light stress proteins in photosynthetic organisms.Crossref | GoogleScholarGoogle Scholar |
Hilbricht T, Varotto S, Sgaramella V, Bartels D, Salamini F, Furini A (2008) Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection in the plant Craterostigma plantagineum. New Phytologist 179, 877–887.
| Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection in the plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar |
Höfler K (1943) Über die Austrocknungsfähigkeit des Protoplasmas. Berichte der deutschen botanischen Geselschaft 60, 94–106.
Höfler K, Migsch H, Rottenburg W (1941) Über die Austrocknungresistenz landwirtschaftlicher Kulturpflanzen. Forschungsdienst 12, 50–61.
Holman R, Brubaker F (1926) On the longevity of pollen. University of California Publications in Botany 13, 179–204.
Illing N, Denby K, Collet H, Shen A, Farrant J (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissue. Integrative and Comparative Biology 45, 771–787.
| The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissue.Crossref | GoogleScholarGoogle Scholar |
Iturriaga G, Gaff D, Zentella R (2000) New desiccation-tolerant plants, including a grass, in the Central Highlands of Mexico, accumulate trehalose. Australian Journal of Botany 48, 153–158.
| New desiccation-tolerant plants, including a grass, in the Central Highlands of Mexico, accumulate trehalose.Crossref | GoogleScholarGoogle Scholar |
Jäger K, Bergman B (1991) Localization of a multifunctional chaperonin (GroEL protein) in nitrogen-fixing Anabaena PCC 7120. Planta 183, 120–125.
| Localization of a multifunctional chaperonin (GroEL protein) in nitrogen-fixing Anabaena PCC 7120.Crossref | GoogleScholarGoogle Scholar |
Kim BH, Schoffl F (2002) Interaction between Arabidopsis heat shock transcription factor 1 and 70kDa heat shock proteins. Journal of Experimental Botany 53, 371–375.
| Interaction between Arabidopsis heat shock transcription factor 1 and 70kDa heat shock proteins.Crossref | GoogleScholarGoogle Scholar |
Kuang J, Gaff D, Gianello R, Blomstedt C, Neale A, Hamill J (1995) Changes in in vivo protein complements in drying leaves of the desiccation-tolerant grass Sporobolus stapfianus and the desiccation-sensitive grass Sporobolus pyramidalis. Australian Journal of Plant Physiology 22, 1027–1034.
| Changes in in vivo protein complements in drying leaves of the desiccation-tolerant grass Sporobolus stapfianus and the desiccation-sensitive grass Sporobolus pyramidalis.Crossref | GoogleScholarGoogle Scholar |
Lebkuecher JG (1997) Desiccation-time limits of photosynthetic recovery in Equisetum hyemale (Equisetaceae) spores. American Journal of Botany 84, 792–797.
| Desiccation-time limits of photosynthetic recovery in Equisetum hyemale (Equisetaceae) spores.Crossref | GoogleScholarGoogle Scholar |
Levitt J, Sullivan CY, Krull E (1960) Some problems in drought resistance. Bulletin of the Research Council of Israel 8D, 177–179.
Liu K, Eastwood RJ, Flynn S, Turner RM, Stuppy WH (2008) ‘Seed information database. (Release 7.1, May 2008)’ Available at http://www.kew.org/data/sid.
Liu X, Wang Z, Wang L, Wu R, Phillips J, Deng X (2009) LEA 4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco. Plant Science 176, 90–98.
| LEA 4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar |
Lüttge U, Beck E, Bartels D, Eds (2011) ‘Plant desiccation tolerance.’ (Springer: Heidelberg, Germany)
Maia J, Dekkers BJW, Provart NJ, Ligterink W, Hilhorst HWM (2011) The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome. PLoS ONE 6, e29123
| The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome.Crossref | GoogleScholarGoogle Scholar |
Martinelli T, Whittaker A, Bochicchio A, Vazzana C, Suzuki A, Masclaux-Daubresse C (2007) Amino acid pattern and glutamate metabolism during dehydration stress in the ‘resurrection’ plant Sporobolus stapfianus: a comparison between desiccation-sensitive and desiccation-tolerant leaves. Journal of Experimental Botany 58, 3037–3046.
| Amino acid pattern and glutamate metabolism during dehydration stress in the ‘resurrection’ plant Sporobolus stapfianus: a comparison between desiccation-sensitive and desiccation-tolerant leaves.Crossref | GoogleScholarGoogle Scholar |
McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends in Ecology & Evolution 19, 661–666.
| Charophyte algae and land plant origins.Crossref | GoogleScholarGoogle Scholar |
Neale A, Blomstedt C, Bronson P, Le T-N, Guthridge K, Evans J, Gaff D, Hamill J (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe stress. Plant, Cell & Environment 23, 265–277.
| The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe stress.Crossref | GoogleScholarGoogle Scholar |
Oliver MJ (2007) Lessons on dehydration tolerance from desiccation-tolerant plants. In ‘Plant desiccation tolerance’. (Eds MA Jenk, AJ Wood) pp. 11–50. (Blackwell: Ames, IA)
Oliver MJ, Bewley JD (1997) Desiccation tolerance of plant tissues: a mechanistic overview. Horticultural Reviews 18, 171–214.
Oliver MJ, Tuba Z, Mishler B (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecology 151, 85–100.
| The evolution of vegetative desiccation tolerance in land plants.Crossref | GoogleScholarGoogle Scholar |
Oliver MJ, Velten J, Mishler B (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integrative and Comparative Biology 45, 788–799.
| Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats?Crossref | GoogleScholarGoogle Scholar |
Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BWM, Cushman JC (2011a) A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. The Plant Cell 23, 1231–1248.
| A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus.Crossref | GoogleScholarGoogle Scholar |
Oliver MJ, Jain R, Balbuena TS, Agrawal G, Gasulla F, Thelen JJ (2011b) Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration. Phytochemistry 72, 1273–1284.
| Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration.Crossref | GoogleScholarGoogle Scholar |
Pate JS, Dixon KW (1982) ‘Tuberous, cormous and bulbous plants — biology of an adaptive strategy.’ (University of Western Australia Press: Nedlands, WA)
Pence VC (2000) Survival of chlorophyllous and nonchlorophyllous fern spores through exposure to liquid nitrogen. American Fern Journal 90, 119–126.
| Survival of chlorophyllous and nonchlorophyllous fern spores through exposure to liquid nitrogen.Crossref | GoogleScholarGoogle Scholar |
Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F (2007) Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. Journal of Experimental Botany 58, 1947–1956.
| Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit.Crossref | GoogleScholarGoogle Scholar |
Petersen J, Eriksson SK, Harryson P, Pierog S, Colby T, Bartels D, Röhrig H (2012) The lysine-rich motif of intrinsically disordered stress protein CdeT11–24 from Craterostigma plantagineum is responsible for phosphatidic acid binding and protection of enzymes from damaging effects caused by desiccation. Journal of Experimental Botany 63, 4919–4929.
| The lysine-rich motif of intrinsically disordered stress protein CdeT11–24 from Craterostigma plantagineum is responsible for phosphatidic acid binding and protection of enzymes from damaging effects caused by desiccation.Crossref | GoogleScholarGoogle Scholar |
Porembski S, Barthlott W (2000) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation tolerant plants. Plant Ecology 151, 19–28.
| Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation tolerant plants.Crossref | GoogleScholarGoogle Scholar |
Prieto-Dapena P, Castaño R, Almoguera C, Jordano J (2008) The ectotopic overexpression of a seed-specific transcription factor, HaHSFA9, confers tolerance to severe dehydration in vegetative organs. The Plant Journal 54, 1004–1014.
| The ectotopic overexpression of a seed-specific transcription factor, HaHSFA9, confers tolerance to severe dehydration in vegetative organs.Crossref | GoogleScholarGoogle Scholar |
Pruzsinsky S (1960) Über Trocken- und Feuchtluftresistenz des Pollen. Osterreichische Akademie der Wissenschaften: Mathematik.-natur Klass., Abteilung 1 169, 43–100.
Raven JA (2002) Selection pressure on stomatal evolution. New Phytologist 153, 371–386.
| Selection pressure on stomatal evolution.Crossref | GoogleScholarGoogle Scholar |
Raven JA, Andrews M (2010) Evolution of tree nutrition. Tree Physiology 30, 1050–1071.
| Evolution of tree nutrition.Crossref | GoogleScholarGoogle Scholar |
Reed R, Richardson DL, Warr S, Stewart WDP (1984) Carbohydrate accumulation and osmotic stress in cyanobacteria. Journal of General Microbiology 130, 1–4.
Rodriguez MCS, Edsgärd D, Hussain SS, Alquezar D, Rasmussen M, Gilbert T, Nielsen BH, Bartels D, Mundy J (2010) Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. The Plant Journal 63, 212–228.
| Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar |
Sallon S, Solowey E, Cohen Y, Korchinsky R, Egli M, Woodhatch I, Simchoni O, Kislev M (2008) Germination, genetics, and growth of an ancient date seed. Science 320, 1464
| Germination, genetics, and growth of an ancient date seed.Crossref | GoogleScholarGoogle Scholar |
Shen Y, Tang M-J, Hu Y-L, Lin Z-P (2004) Isolation and characterization of a dehydrin-like gene from drought-tolerant Boea crassifolia. Plant Science 166, 1167–1175.
Thompson MD, Paavola CD, Lenvik TR, Gantt JS (1995) Chlamydomonas transcripts encoding three divergent plastid chaperonins are heat-inducible. Plant Molecular Biology 27, 1031–1035.
| Chlamydomonas transcripts encoding three divergent plastid chaperonins are heat-inducible.Crossref | GoogleScholarGoogle Scholar |
Tietz A, Ruttkowski U, Köhler R, Kasprik W (1989) Further investigations on the occurrence and the effects of abscisic acid in algae. Biochemie und Physiologie der Pflanzen 184, 259–266.
Van Zanten B (1978) Experimental studies on the trans oceanic long-range dispersal of moss spores in the southern hemisphere. Journal of the Hattori Botanical Laboratory 44, 455–482.
Visser T (1955) Germination and storage of pollen. Meded Landbouwhogeschool Wageningen 55, 1–68.
Watkins JE, Mack MC, Sinclair TR, Mulkey SS (2007) Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes. New Phytologist 176, 708–717.
| Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes.Crossref | GoogleScholarGoogle Scholar |
Wehmeyer N, Vierling E (2000) The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiology 122, 1099–1108.
| The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance.Crossref | GoogleScholarGoogle Scholar |
Werner O, Ros-Espin R, Bopp M, Atzorn R (1991) Abscisic acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186, 99–103.
| Abscisic acid-induced drought tolerance in Funaria hygrometrica Hedw.Crossref | GoogleScholarGoogle Scholar |
Yobi A, Wone BWM, Xu W, Alexander DC, Guo L, Ryals JA, Oliver MJ, Cushman JC (2012) Comparative metabolic profiling between desiccation sensitive and desiccation tolerant species of Selaginella reveals novel insights into the resurrection trait. The Plant Journal 72, 983–999.
| Comparative metabolic profiling between desiccation sensitive and desiccation tolerant species of Selaginella reveals novel insights into the resurrection trait.Crossref | GoogleScholarGoogle Scholar |
Yokota T, Kim SK, Fukui Y, Takahashi N, Takeuchi Y, Takematsu T (1987) Brassinosteroids and sterols from a green alga Hydrodictyon reticulatum: Configuration at C-24. Phytochemistry 26, 503–506.
| Brassinosteroids and sterols from a green alga Hydrodictyon reticulatum: Configuration at C-24.Crossref | GoogleScholarGoogle Scholar |
Zahradníčková H, Marðálek B, Poliðenská M (1991) High-performance thin-layer chromatographic and high-performance liquid chromatographic determination of abscisic acid produced by cyanobacteria. Journal of Chromatography. ,A 555, 239–245.
| High-performance thin-layer chromatographic and high-performance liquid chromatographic determination of abscisic acid produced by cyanobacteria.Crossref | GoogleScholarGoogle Scholar |