A field portable method for the semi-quantitative estimation of dehydration tolerance of photosynthetic tissues across distantly related land plants.


Journal

Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322

Informations de publication

Date de publication:
Dec 2019
Historique:
received: 27 10 2018
revised: 21 11 2018
accepted: 28 11 2018
pubmed: 6 12 2018
medline: 10 3 2020
entrez: 6 12 2018
Statut: ppublish

Résumé

Desiccation tolerant (DT) plants withstand complete cellular dehydration, reaching relative water contents (RWC) below 30% in their photosynthetic tissues. Desiccation sensitive (DS) plants exhibit different degrees of dehydration tolerance (DHT), never surviving water loss >70%. To date, no procedure for the quantitative evaluation of DHT extent exists that is able to discriminate DS species with differing degrees of DHT from truly DT plants. We developed a simple, feasible and portable protocol to differentiate between DT and different degrees of DHT in the photosynthetic tissues of seed plants and between fast desiccation (< 24 h) tolerant (FDT) and sensitive (FDS) bryophytes. The protocol is based on (1) controlled desiccation inside Falcon tubes equilibrated at three different relative humidities that, consequently, induce three different speeds and extents of dehydration and (2) an evaluation of the average percentage of maximal photochemical efficiency of PSII (F

Identifiants

pubmed: 30515832
doi: 10.1111/ppl.12890
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

540-555

Subventions

Organisme : Basque Government
ID : UPV/EHU IT-1018-16
Organisme : Spanish Ministry of Economy and Competitiveness (MINECO)
ID : BES-2015-072578
Organisme : ERDF (FEDER)
ID : CTM2014-53902-C2-2-P
Organisme : ERDF (FEDER)
ID : CGL2014-54127-P
Organisme : ERDF (FEDER)
ID : CTM2014-53902-C2-1-P
Organisme : Juan de la Cierva-Incorporation fellowship
ID : 2014-22489
Organisme : Juan de la Cierva-Formación
ID : FPDI-2013-18167
Organisme : Juan de la Cierva-Formación
ID : FPDI-2013-17135
Organisme : Conselleria d'Educació, Cultura i Universitats
ID : FPI/1700/2014
Organisme : ESF
Organisme : Spanish Ministry of Education, Culture and Sport (MECD) fellowship
ID : FPU15/02054
Organisme : South African Department of Science and Technology and National Research Foundation
ID : 98406

Informations de copyright

© 2018 Scandinavian Plant Physiology Society.

Références

Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45: 685-695
Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209: 1575-1584
Bartoskova H, Komenda J, Naus J (1999) Functional changes of photosystem II in the moss Rhizomnium punctatum (Hedw.) induced by different rates of dark desiccation. J Plant Physiol 154: 597-604
Bewley JD (1979) Physiological aspects of desiccation tolerance. Annu Rev Plant Physiol 30: 195-238
Blum A, Tuberosa R (2018) Dehydration survival in crop plants and its measurement. J Exp Bot 69: 975-981
Boothby TC, Tapia H, Brozena AH, Piszkiewicz S, Smith AE, Giovannini I, Rebecchi L, Pielak GJ, Koshland D, Goldstein B (2017) Tardigrades use intrinsically disordered proteins to survive desiccation. Mol Cell 65: 975-984
Buda GJ, Barnes WJ, Fich EA, Park S, Yeats TH, Zhao L, Domozych DS, Rose JKC (2013) An ATP binding cassette transporter is required for cuticular wax deposition and desiccation tolerance in the moss Physcomitrella patens. Plant Cell 25: 4000-4013
Candotto Carniel F, Zanelli D, Bertuzzi S, Tretiach M (2015) Desiccation tolerance and lichenization: a case study with the aeroterrestrial microalga Trebouxia sp. (Chlorophyta). Planta 242: 493-505
Carriquí M, Cabrera HM, Conesa MÀ, Coopman RE, Douthe C, Gago J, Gallé A, Galmés J, Ribas-Carbó M, Tomàs M, Flexas J (2015) Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study. Plant Cell Environ 38: 448-460
Cruz de Cargalho R, Bernardes da Silva A, Soares R, Almeida AM, Coleho AV, Marques de Silva J, Branquinho C (2014) Differential proteomics of dehydration and rehydration in bryophytes: evidence towards a common desiccation tolerance mechanism. Plant Cell Environ 37: 1499-1515
Cruz de Carvalho R, Branquinho C, Da Silva JM (2011) Physiological consequences of desiccation in the aquatic bryophyte Fontinalis antipyretica. Planta 234: 195-205
Cruz de Carvalho R, Catalá M, Da Silva JM, Branquinho C, Barreno E (2012) The impact of dehydration rate on the production and cellular location of reactive oxygen species in an aquatic moss. Ann Bot 110: 1007-1016
Cruz de Carvalho R, Catalá M, Branquinho C, da Silva JM, Barreno E (2017) Dehydration rate determines the degree of membrane damage and desiccation tolerance in bryophytes. Physiol Plant 159: 277-289
Deltoro V, Calatayud A, Gimeno C, Barreno E (1998) Water relations, chlorophyll fluorescence, and membrane permeability during desiccation in bryophytes from xeric, Mesic, and hydric environments. Can J Bot 76: 1923-1929
Dinakar C, Djilianov D, Bartels D (2012) Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defence. Plant Sci 182: 29-41
Esteban R, Balaguer L, Manrique E, Rubio de Casas R, Ochoa O, Fleck I, Pintó-Marijuan M, Casals I, Morales D, Jiménez MS, Lorenzo R, Artetxe U, Becerril JM, García-Plazaola JI (2009) Alternative methods for sampling and preservation of photosynthetic pigments and tocopherols in plant material from remote locations. Photosynth Res 101: 77-88
Farrant JM, Moore JP (2011) Programming desiccation-tolerance: from plants to seeds to resurrection plants. Curr Opin Plant Biol 14: 340-345
Farrant JM, Cooper K, Kruger LA, Sherwin HW (1999) The effect of drying rate on the survival of three desiccation-tolerant angiosperm species. Ann Bot 84: 371-379
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
Farrant JM, Cooper K, Hilgart A, Abdalla KO, Bentley J, Thomson JA, Dace HJW, Peton N, Mundree SG, Rafudeen MS (2015) A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (baker). Planta 242: 407-426
Farrant JM, Cooper K, Dace HJW, Bentley J, Hilgart A (2017) Desiccation tolerance. In: Shabala S (ed) Plant Stress Physiology, 2nd Edn. CAB International, Croydon, pp 217-252
Fernández-Marín B, Balaguer L, Esteban R, Becerril JM, García-Plazaola JI (2009) Dark induction of the photoprotective xanthophyll cycle in response to dehydration. J Plant Physiol 166: 1734-1744
Fernández-Marín B, Becerril JM, García-Plazaola JI (2010) Unravelling the roles of desiccation-induced xanthophyll cycle activity in darkness: a case study in Lobaria pulmonaria. Planta 231: 1335-1342
Fernández-Marín B, Míguez F, Becerril JM, García-Plazaola JI (2011) Dehydration-mediated activation of the xanthophyll cycle in darkness: is it related to desiccation tolerance? Planta 243: 579-588
Fernández-Marín B, Kranner I, San Sebastián M, Artetxe U, Laza JM, Vilas JL, Pritchard HW, Nadajaran J, Míguez F, Becerril J, García-Plazaola JI (2013) Evidence for the absence of enzymatic reactions in the glassy state. A case study of xanthophyll cycle pigments in the desiccation-tolerant moss Syntrichia ruralis. J Exp Bot 64: 3033-3043
Fernández-Marín B, Holzinger A, Garcia-Plazaola JI (2016) Photosynthetic strategies of desiccation-tolerant organisms. In: Pessarakli M (ed) Handbook of Photosynthesis, 3rd Edn. CRC Press, Boca Raton, pp 719-737
Fernández-Marín B, Neuner G, Kuprian E, Laza JM, García-Plazaola JI, Verhoeven A (2018) First evidence of freezing tolerance in a resurrection plant: insights into molecular mobility and zeaxanthin synthesis in the dark. Physiol Plant 163: 472-489
Gaff DF (1977) Desiccation tolerant vascular plants of southern Africa. Oecologia 31: 95-109
Gaff DF (1989) Responses of desiccation tolerant resurrection plants to water stress. In: Kreeb KH, Richter H, Hinckley TM (eds) Structural and Functional Responses to Environmental Stresses. SPB Academic Publishing, The Hague, pp 264-311
Gaff DF, Loveys BR (1992) Abscisic acid levels in drying plants of a resurrection grass. Trans Malaysian Soc Plant Physiol 3: 286-287
Gaff DF, Oliver M (2013) The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct Plant Biol 40: 315-328
Gasulla F, de Nova PG, Esteban-Carrasco A, Zapata JM, Barreno E, Guéra A (2009) Dehydration rate and time of desiccation affect recovery of the lichen alga Trebouxia erici: alternative and classical protective mechanisms. Planta 23: 195-208
Gauslaa Y, Coxson DS, Solhaug KA (2012) The paradox of higher light tolerance during desiccation in rare old forest cyanolichens than in more widespread co-occurring chloro- and cephalolichens. New Phytol 195: 812-822
Giarola V, Hou Q, Bartels D (2017) Angiosperm plant desiccation tolerance: hints from transcriptomics and genome sequencing. Trends Plant Sci 22: 705-717
Ginbot ZG, Farrant JM (2011) Physiological response of selected Eragrostis species to water-deficit stress. Afr J Biotechnol 10: 10405-10417
Griffiths CA, Gaff DF, Neale AD (2014) Drying without senescence in resurrection plants. Front Plant Sci 5: 36
Guéra A (2009) Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta 231: 195-208
Gupta RK (1977) A note on photosynthesis in relation to water content in liverworts: Porella platyphylla and Scapania undulata. Aust J Bot 25: 363-365
Hajek T, Vicherova E (2014) Desiccation tolerance of Sphagnum revisited: a puzzle resolved. Plant Biol 16: 765-773
Heber U, Shuvalov VA (2005) Photochemical reactions of chlorophyll in dehydrated photosystem II: two chlorophyll forms (680 and 700 nm). Photosynth Res 84: 85-91
Hellwege EM, Dietz KJ, Volk OH, Hartung W (1994) Abscisic acid and the induction of desiccation tolerance in the extremely xerophylic liverwort Exormotheca holstii. Planta 194: 525-531
Hoekstra (2005) Differential longevities in desiccated anhydrobiotic plant systems. Integr Comp Biol 45: 725-733
Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6: 431-438
Höfler K (1941) Uber die austrocknungsfahigkeit des protoplasmas. Ber Dtsch Bot Ges 60: 94-106
Hong TD, Linington SH, Ellis RH (1998) Compendium of Information of Seed Storage Behaviour. Royal Botanic Gardens, Kew, pp. 901
Kopecky J, Azarkovich M, Pfündel EE, Shuvalov VA, Heber U (2005) Thermal dissipation of light energy is regulated differently and by different mechanisms in lichens and higher plants. Plant Biol 7: 156-167
Koster KL, Balsamo RA, Espinoza C, Oliver MJ (2010) Desiccation sensitivity and tolerance in the moss Physcomitrella patens: assessing limits and damage. Plant Growth Regul 62: 293-302
Kranner I, Beckett R, Hochman A, Nash TH (2008) Desiccation tolerance in lichens: a review. Bryologist 11: 576-593
Lidén M, Cabrajic AVJ, Ottosson-Löfvenius M, Palmquist K, Lundmark T (2010) Species-specific activation time-lags can explain habitat restrictions in hydrophilic lichens. Plant Cell Environ 33: 851-862
Lizarazo K, Fernández-Marín B, Becerril JM, García-Plazaola JI (2010) Ageing and irradiance enhance vitamin E content in green edible tissues from crop plants. J Sci Food Agric 90: 1994-1999
López-Pozo M, Fernández-Marín B, García-Plazaola JI, Ballesteros D (2018) Desiccation tolerance in ferns: from the unicellular spore to the multi-tissular sporophyte. In: Fernández H (ed) Current Advances in Fern Research. Springer International Publishing AG, Cham, Switzerland, pp 401-426
Marks TR, Seaton PT, Pritchard HW (2014) Desiccation tolerance, longevity and seed-siring ability of entomophilous pollen from UKnative orchid species. Ann Bot 114: 561-569
Moore JP, Nguema-Ona EE, Vicre-Gibouin M, Sorensen I, Willats WGT, Driouich A, Farrant JM (2013) Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237: 739-754
Pandey V, Ranjan S, Deeba F, Pandey AK, Singh R, Shirke PA, Pathre UV (2010) Desiccation-induced physiological and biochemical changes in resurrection plant, Selaginella bryopteris. J Plant Physiol 167: 1351-1359
Pence VC, Dunford SS, Redella S (2005) Differential effects of abscisic acid on desiccation tolerance and carbohydrates in three species of liverworts. J Plant Physiol 162: 1331-1337
Pérez P, Rabnez G, Laufer Z, Gutiérrez D, Tuba Z, Martínez-Carrasco R (2011) Restoration of photosystem II photochemistry and carbon assimilation and related changes in chlorophyll and protein contents during the rehydration for desiccated Xerophyta scabrida leaves. J Exp Bot 62: 895-905
Pittermann J, Limm E, Rico C, Christman MA (2011) Structure-function constraints of tracheid-based xylem: a comparison of conifers and ferns. New Phytol 192: 449-461
Porembski S (2011) Evolution, diversity and habitats of poikilohydrous vascular plants. In: Luttge U, Beck E, Bartels D (eds) Plant Desiccation Tolerance. Springer Science & Business, Berlin, Germany, pp p139-p156
Proctor MCF (2009) Desiccation tolerance in some British ferns. Fern Gaz 18: 264-282
Proctor MCF (2010) Recovery rates of chlorophyll-fluorescence parameters in desiccation-tolerant plants: fitted logistic curves as a versatile and robust source of comparative data. Plant Growth Regul 62: 233-240
Proctor MCF, Ligrone R, Duckett JG (2007a) Desiccation tolerance in the moss Polytrichum formosum: physiological and fine-structural changes during desiccation and recovery. Ann Bot 99: 75-93
Proctor MCF, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD (2007b) Desiccation-tolerance in bryophytes: a review. Bryologist 110: 595-621
Rakić T, Lazarević M, Jovanović ŽS, Radović S, Siljak-Yakolev S, Stevanović B, Stevanović V (2014) Resurrection plants of the genus Ramonda: prospective survival strategies - unlock further capacity of adaptation, or embark on the path of evolution. Front Plant Sci 4: 550
Riaño K, Briones O (2015) Sensitivity of three tree ferns during their first phase of life to the variation of solar radiation and water availability in a Mexican cloud forest. Am J Bot 102: 1472-1481
Saldaña A, Parra MJ, Flores-Bavestrello A, Corcuera LJ, Bravo LA (2013) Effects of forest successional status on microenvironmental conditions, diversity, and distribution of filmy fern species in a temperate rainforest. Plant Species Biol 29: 253-262
Schonbeck MW, Bewley JD (1981) Responses of the moss Tortula ruralis to desiccation treatments. I. Effects of minimum water content and rates of dehydration and rehydration. Can J Bot 59: 2698-2706
Sherwin HW, Farrant JM (1996) Differences in rehydration of three desiccation-tolerant angiosperm species. Ann Bot 78: 703-710
Sherwin HW, Farrant JM (1998) Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regul 24: 203-210
Sherwin HW, Pammenter NW, February ED, Vander Willigen C, Farrant JM (1998) Xylem hydraulic characteristics, water relations and wood anatomy of the resurrection plant Myrothamnus flabellifolius Welw. Ann Bot 81: 567-575
Slate ML, Stark LR, Greenwood JL, Clark TA, Brinda JC (2018) The role of prehydfration in rescuing shoots of mosses damaged by extreme desiccation events: Syntrichia norvegica (Pottiaceae). Bryologist 121: 193-204
Stark LR (2017) Ecology of desiccation tolerance in bryophytes: a conceptual framework and methodology. The Bryologist 120: 130-165
Stark LR, Brinda JC, Greenwood JL (2016) Propagula and shoots of Syntrichia pagorum (Pottiaceae) exhibit different ecological strategies of desiccation tolerance. Bryologist 119: 181-192
Stark LR, Greenwood JL, Brinda JC, Oliver MJ (2013a) Physiological history may mask the inherent inducible desiccation tolerance strategy of the desert moss Crossidium crassinerve. Plant Biol 16: 935-946
Stark LR, Greenwood JL, Brinda JC, Oliver MJ (2013b) The desert moss Pterygoneurum lamellatum (Pottiaceae) exhibits an inducible ecological strategy of desiccation tolerance: effects of rate of drying on shoot damage and regeneration. Am J Bot 100: 1522-1531
Stark LR, Greewood JL, Slate ML, Brinda C (2017) Syntrichia norvegica shoots exhibit a complex inducible response to desiccation: separating the effects of rate of drying and water content. Botany 95: 481-491
Suguiyama VF, Silva EA, Meirelles ST, Centeno DC, 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
Tosens T, Niinemets Ü, Westoby M, Wright I (2012) Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. J Exp Bot 63: 5105-5119
Tuba Z, Lichtenthaler K (2011) Ecophysiology of homoiochlorophyllous and poikilochlorophyllous desiccation-tolerant plants and vegetations. In: Lüttge U, Beck E, Bartels D (eds) Plant Desiccation Tolerance. Springer, London, UK, pp 157-184
Tuba Z, Csintalan Z, Proctor MCF (1996) Photosynthetic responses of a moss, Tortula ruralis, ssp. ruralis, and the lichens Cladonia convoluta and C. furcata to water deficit and short periods of desiccation, and their ecophysiological significance: a baseline study at present-day CO2 concentration. New Phytol 133: 353-361
Verhoeven A, García-Plazaola JI, Fernández-Marín B (2018) Shared mechanisms of photoprotection in photosynthetic organisms tolerant to desiccation or to low temperature. Environ Exp Bot 154: 66-79. https://doi.org/10.1016/j.envexpbot.2017.09.012
Vicré M, Farrant JM, Driouich A (2004) Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species. Plant Cell Environ 27: 1329-1340
Wagner HJ, Schneider H, Mimietz S, Wistuba N, Rokitta M, Krohne G, Haase A, Zimmermann U (2000) Xylem conduits of a resurrection plant contain a unique lipid lining and refill following a distinct pattern after desiccation. New Phytol 148: 239-255
Whittaker A, Martinelly T, Bochicchio A, Vazzana C, Farrant J (2004) Comparison of sucrose metabolism during the rehydration of desiccation-tolerant and desiccation-sensitive leaf material of Sporobolus stapfianus. Physiol Plant 122: 11-20
Wood AJ (2007) The nature and distribution of vegetative desiccation-tolerance in hornworts, liverworts and mosses. Bryologist 110: 163-177
Xiao L, Yobi A, Koster KL, He Y, Oliver MJ (2018) Desiccation tolerance in Physcomitrella patens: rate of dehydration and the involvement of endogenous abscisic acid (ABA). Plant Cell Environ 41: 275-284
Zhang Q, Bartels D (2018) Molecular responses to dehydration and desiccation in desiccation-tolerant angiosperm plants. J Exp Bot 69: 3211-3222

Auteurs

Marina López-Pozo (M)

Department Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Leioa, Spain.

Jaume Flexas (J)

Research Group on Plant Biology under Mediterranean conditions, Departament de Biologia, Universitat de les Illes Balears/Institute of Agro-Environmental and Water Economy Research -INAGEA, Palma, Spain.

Javier Gulías (J)

Research Group on Plant Biology under Mediterranean conditions, Departament de Biologia, Universitat de les Illes Balears/Institute of Agro-Environmental and Water Economy Research -INAGEA, Palma, Spain.

Marc Carriquí (M)

Research Group on Plant Biology under Mediterranean conditions, Departament de Biologia, Universitat de les Illes Balears/Institute of Agro-Environmental and Water Economy Research -INAGEA, Palma, Spain.

Miquel Nadal (M)

Research Group on Plant Biology under Mediterranean conditions, Departament de Biologia, Universitat de les Illes Balears/Institute of Agro-Environmental and Water Economy Research -INAGEA, Palma, Spain.

Alicia V Perera-Castro (AV)

Research Group on Plant Biology under Mediterranean conditions, Departament de Biologia, Universitat de les Illes Balears/Institute of Agro-Environmental and Water Economy Research -INAGEA, Palma, Spain.

María José Clemente-Moreno (MJ)

Research Group on Plant Biology under Mediterranean conditions, Departament de Biologia, Universitat de les Illes Balears/Institute of Agro-Environmental and Water Economy Research -INAGEA, Palma, Spain.

Jorge Gago (J)

Research Group on Plant Biology under Mediterranean conditions, Departament de Biologia, Universitat de les Illes Balears/Institute of Agro-Environmental and Water Economy Research -INAGEA, Palma, Spain.

Encarnación Núñez-Olivera (E)

University of La Rioja, Facultad de Ciencia y Tecnología, Logroño, Spain.

Javier Martínez-Abaigar (J)

University of La Rioja, Facultad de Ciencia y Tecnología, Logroño, Spain.

Antonio Hernández (A)

Department Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Leioa, Spain.

Unai Artetxe (U)

Department Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Leioa, Spain.

Joanne Bentley (J)

Department of Molecular and Cell Biology, University of Cape Town, Rondebosch, South Africa.

Jill M Farrant (JM)

Department of Molecular and Cell Biology, University of Cape Town, Rondebosch, South Africa.

Amy Verhoeven (A)

Biology Department (OWS352), University of St. Thomas, St. Paul, MN, USA.

José Ignacio García-Plazaola (JI)

Department Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Leioa, Spain.

Beatriz Fernández-Marín (B)

Department Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Leioa, Spain.

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