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Comparative physiological and proteomic analyses reveal different adaptive strategies by Cymbidium sinense and C. tracyanum to drought

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Abstract

Main conclusion

A terrestrial orchid, Cymbidium sinense appears to utilizes “remedy strategy”, while an epiphytic orchid, C. tracyanum , employs a “precaution strategy” to drought stress based on morphological, physiological and proteomic analysis.

Drought condition influences plant growth and productivity. Although the mechanism by which plants adapt to this abiotic stress has been studied extensively, the water-adaptive strategies of epiphytes grown in water-limited habitats remain undefined. Here, root and leaf anatomies, dynamic changes in physiological and proteomic responses during periods of drought stress and recovery studied in an epiphytic orchid (Cymbidium tracyanum) and a terrestrial orchid (C. sinense) to investigate their strategies for coping with drought. Compared with C. sinense, C. tracyanum showed stronger drought-resistant adaptive characteristics to drought because its leaves had more negative water potential at turgor loss point and roots had higher proportion of velamen radicum thickness. Although both species demonstrated quick recovery of photosynthesis after stress treatment, they differed in physiological and proteomic responses. We detected and functionally characterized 103 differentially expressed proteins in C. sinense and 104 proteins in C. tracyanum. These proteins were mainly involved in carbon and energy metabolism, photosynthesis, and defense responses. The up-regulated expression of plastid fibrillin may have contributed to the marked accumulation of jasmonates only in stressed C. sinense, while ferredoxin-NADP reductase up-regulation was only found in C. tracyanum which possibly related to the stimulation of cyclic electron flow that is linked with photoprotection. These physiological and proteomic performances suggest distinct adaptive strategies to drought stress between C. sinense (remedy strategy) and C. tracyanum (precaution strategy). Our findings may help improve our understanding about the ecological adaptation of epiphytic orchids.

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Abbreviations

A n :

Net photosynthesis

g s :

Stomatal conductance

Ψ MD :

Midday leaf water content

F v/F m :

Maximum quantum yield of PSII after dark adaptation overnight

P m :

Maximum photo-oxidizable P700

CEF:

Cyclic electron flow

JA:

Jasmonates

ABA:

Abscisic acid

References

  • Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233

    Article  CAS  Google Scholar 

  • Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277:2006–2011

    Article  CAS  PubMed  Google Scholar 

  • Benzing D, Ott D, Friedman W (1982) Roots of Sobralia macrantha (Orchidaceae): structure and function of the velamen-exodermis complex. Am J Bot 69:608–614

    Article  Google Scholar 

  • Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123

    Article  PubMed  Google Scholar 

  • Bonhomme L, Monclus R, Vincent D, Carpin S, Lomenech AM, Plomion C, Brignolas F, Morabito D (2009) Leaf proteome analysis of eight Populus × euramericana genotypes: genetic variation in drought response and in water-use efficiency involves photosynthesis-related proteins. Proteomics 9:4121–4142

    Article  CAS  PubMed  Google Scholar 

  • Brodribb T, Holbrook N, Edwards E, Gutierrez M (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450

    Article  Google Scholar 

  • Chaves M, Oliveira M (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384

    Article  CAS  PubMed  Google Scholar 

  • Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osorio ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. photosynthesis and growth. Ann Bot 89:907–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix JD, Zito F, Forti G (2002) Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep 3:280–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fulda S, Mikkat S, Stegmann H, Horn R (2011) Physiology and proteomics of drought stress acclimation in sunflower (Helianthus annuus L.). Plant Biol 13:632–642

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Hajheidari M, Abdollahian-Noghabi M, Askari H, Heidari M, Sadeghian SY, Ober ES, Hosseini Salekdeh G (2005) Proteome analysis of sugar beet leaves under drought stress. Proteomics 5:950–960

    Article  CAS  PubMed  Google Scholar 

  • Hao GY, Sack L, Wang AY, Cao KF, Goldstein G (2010) Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Funct Ecol 24:731–740

    Article  Google Scholar 

  • Hossain MM, Kant R, Van PT, Winarto B, Zeng S, Teixeira da Silva JA (2013) The application of biotechnology to orchids. Crit Rev Plant Sci 32:69–139

    Article  CAS  Google Scholar 

  • Huang W, Fu P-L, Jiang YJ, Zhang JL, Zhang SB, Hu H, Cao KF (2013) Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia exposed to a prolonged drought in a tropical limestone forest. Tree Physiol 33:e220

    Article  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213

    Article  CAS  PubMed  Google Scholar 

  • James HE, Bartling D, Musgrove J, Kirwin P, Herrmann R, Robinson C (1989) Transport of proteins into chloroplasts. Import and maturation of precursors to the 33-, 23-, and 16-kDa proteins of the photosynthetic oxygen-evolving complex. J Biol Chem 264:19573–19576

    CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  PubMed  Google Scholar 

  • Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Funct Ecol 28:1313–1320

    Article  Google Scholar 

  • Kozlowski T, Pallardy S (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334

    Article  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantitation. Methods Mol Biol 32:9–15

    CAS  PubMed  Google Scholar 

  • Kuang M, Zhang SB (2015) Physiological response to high light in Cymbidium tracyanum and C.sinense. Plant Divers Resour 37:55–62

    Google Scholar 

  • Lehtimäki N, Lintala M, Allahverdiyeva Y, Aro EM, Mulo P (2010) Drought stress-induced upregulation of components involved in ferredoxin-dependent cyclic electron transfer. J Plant Physiol 167:1018–1022

    Article  PubMed  Google Scholar 

  • Li JW, Zhang SB (2016) Differences in the responses of photosystems I and II in Cymbidium sinense and C. tracyanum to long-term chilling stress. Front Plant Sci 6:1097

    PubMed  PubMed Central  Google Scholar 

  • Li MH, Xiao WF, Shi P, Wang SG, Zhong YD, Liu XL, Wang XD, Cai XH, Shi ZM (2008) Nitrogen and carbon source-sink relationships in trees at the Himalayan treelines compared with lower elevations. Plant Cell Environ 31:1377–1387

    Article  CAS  PubMed  Google Scholar 

  • Li X, Yang Y, Sun X, Lin H, Chen J, Ren J, Hu X, Yang Y (2014) Comparative physiological and proteomic analyses of poplar (Populus yunnanensis) plantlets exposed to high temperature and drought. PLoS One 9:e107605

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Chen L, Liu K, Li L, Zhang Y, Huang L (2009) Climate warming brings about extinction tendency in wild population of Cymbidium sinense. Acta Ecol Sin 29:3443–3455

    Google Scholar 

  • Luo Y, Jia J, Wang C (2002) A general review of the conservation status of Chinese orchids. Chin Biodivers 11:70–77

    Google Scholar 

  • Manavalan LP, Guttikonda SK, Tran LSP, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276

    Article  CAS  PubMed  Google Scholar 

  • McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  PubMed  Google Scholar 

  • Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27:64–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, Tomizawa K (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830

    Article  CAS  PubMed  Google Scholar 

  • Motomura H, Yukawa T, Ueno O, Kagawa A (2008) The occurrence of crassulacean acid metabolism in Cymbidium (Orchidaceae) and its ecological and evolutionary implications. J Plant Res 121:163–177

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim et Biophys Acta-Bioenerg 1757:742–749

    Article  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Ogburn R, Edwards EJ (2012) Quantifying succulence: a rapid, physiologically meaningful metric of plant water storage. Plant Cell Environ 35:1533–1542

    Article  PubMed  Google Scholar 

  • Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494–8499

    Article  CAS  PubMed  Google Scholar 

  • Pan R, Zheng X, Wen Z (1993) Change of water physiology of Cymbidium sinense during soil drought period. Acta Bot Yunnanica 16:379–384

    Google Scholar 

  • Pinheiro C, Chaves MM, Ricardo CP (2001) Alterations in carbon and nitrogen metabolism induced by water deficit in the stems and leaves of Lupinus albus L. J Exp Bot 52:1063–1070

    Article  CAS  PubMed  Google Scholar 

  • Porembski S, Barthlott W (1988) Velamen radicum micromorphology and classification of Orchidaceae. Nord J Bot 8:117–137

    Article  Google Scholar 

  • Price AH, Cairns JE, Horton P, Jones HG, Griffiths H (2002) Linking drought-resistance mechanisms to drought avoidance in upland rice using a QTL approach: progress and new opportunities to integrate stomatal and mesophyll responses. J Exp Bot 53:989–1004

    Article  CAS  PubMed  Google Scholar 

  • Ramel F, Sulmon C, Gouesbet G, Couée I (2009) Natural variation reveals relationships between pre-stress carbohydrate nutritional status and subsequent responses to xenobiotic and oxidative stress in Arabidopsis thaliana. Ann Bot 104:1323–1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  CAS  Google Scholar 

  • Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A (2015) Exploring jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 6:1077

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakamoto W, Tamura T, Hanba-Tomita Y, Murata M (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7:769–780

    Article  CAS  PubMed  Google Scholar 

  • Seifter S, Dayton S, Novic B, Muntwyler E (1949) The estimation of glycogen with the anthrone reagent. Biochemistry 25:191–220

    Google Scholar 

  • Shin M, Arnon DI (1965) Enzymic mechanisms of pyridine nucleotide reduction in chloroplasts. J Biol Chem 240:1405–1411

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–475

    Article  CAS  PubMed  Google Scholar 

  • Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate-and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Bauwe H, Badger M (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol 144:487–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419–432

    Article  Google Scholar 

  • Théry M (2001) Forest light and its influence on habitat selection. In: Linsenmair KE, Davis AJ, Fiala B, Speight MR (eds) Tropical forest canopies: ecology and management. Springer, Dordrecht, pp 251–261

    Chapter  Google Scholar 

  • Tikkanen M, Mekala NR, Aro E-M (2014) Photosystem II photoinhibition-repair cycle protects photosystem I from irreversible damage. Biochim et Biophys Acta -Bioenerg 1837:210–215

    Article  CAS  Google Scholar 

  • Tyree M, Hammel H (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot 23:267–282

    Article  Google Scholar 

  • Vallon O, Bulte L, Dainese P, Olive J, Bassi R, Wollman F-A (1991) Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci 88:8262–8266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ (2012) Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot 63:3499–3509

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Chen J, Liu Q, Ben CC, Todd CD, Shi J, Yang Y, Hu X (2012) Comparative proteomic analysis of the thermotolerant plant Portulaca oleracea acclimation to combined high temperature and humidity stress. J Proteome Res 11:3605–3623

    Article  CAS  PubMed  Google Scholar 

  • Yordanov I, Velikova V, Tsonev T (2000) Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38:171–186

    Article  CAS  Google Scholar 

  • Yoshioka M, Uchida S, Mori H, Komayama K, Ohira S, Morita N, Nakanishi T, Yamamoto Y (2006) Quality control of photosystem II cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress. J Biol Chem 281:21660–21669

    Article  CAS  PubMed  Google Scholar 

  • Youssef A, Laizet Yh, Block MA, Maréchal E, Alcaraz JP, Larson TR, Pontier D, Gaffé J, Kuntz M (2010) Plant lipid-associated fibrillin proteins condition jasmonate production under photosynthetic stress. Plant J 61:436–445

    Article  CAS  PubMed  Google Scholar 

  • Yukawa T, Stern WL (2002) Comparative vegetative anatomy and systematics of Cymbidium (Cymbidieae: Orchidaceae). Bot J Linn Soc 138:383–419

    Article  Google Scholar 

  • Zhang M, Sun C, Hao G, Ye X, Liang C, Zhu G (2001) A preliminary analysis of phylogenetic relationships in Cymbidium (Orchidaceae) based on nrITS sequence data. Acta Bot Sin 44:588–592

    Google Scholar 

  • Zhang SB, Dai Y, Hao GY, Li JW, Fu XW, Zhang JL (2015) Differentiation of water-related traits in terrestrial and epiphytic Cymbidium species. Front Plant Sci 6:260

    PubMed  PubMed Central  Google Scholar 

  • Zhang W, Hu H, Zhang SB (2016) Divergent adaptive strategies by two co-occurring epiphytic orchids to water stress: escape or avoidance? Front Plant Sci 7:588

    PubMed  PubMed Central  Google Scholar 

  • Zotz G, Bader M (2009) Epiphytic plants in a changing world: global change effects on vascular and non-vascular epiphytes. In: Canovas FM, Luttge U, Matyssek R (eds) Progress in botany. Springer, Dordrecht, pp 147–170

    Chapter  Google Scholar 

  • Zotz G, Hietz P (2001) The physiological ecology of vascular epiphytes: current knowledge, open questions. J Exp Bot 52:2067–2078

    Article  CAS  PubMed  Google Scholar 

  • Zotz G, Tyree MT (1996) Water stress in the epiphytic orchid, Dimerandra emarginata (G. Meyer) Hoehne. Oecologia 107:151–159

    Article  PubMed  Google Scholar 

  • Zotz G, Winkler U (2013) Aerial roots of epiphytic orchids: the velamen radicum and its role in water and nutrient uptake. Oecologia 171:733–741

    Article  PubMed  Google Scholar 

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Acknowledgements

This work is financially supported by the National Natural Science Foundation of China (31370362, 31670342), and National Key Project of the Ministry of Science and Technology of China (2015BAD10B03).

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Authors and Affiliations

  1. Key Laboratory for Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, Kunming, 650201, Yunnan, China

    Jia-Wei Li, Lan Ma & Shi-Bao Zhang

  2. Yunnan Key Laboratory for Wild Plant Resources, Kunming, 650201, China

    Jia-Wei Li, Lan Ma & Shi-Bao Zhang

  3. College of Life Science, Shanghai University, Shanghai, 200444, China

    Xiang-Yang Hu

  4. College of Life Science, University of Chinese Academy of Sciences, Beijing, 100049, China

    Jia-Wei Li

  5. School of Environmental and Biological Engineering, Nanjing University of Science and Technology, Nanjing, 210094, China

    Xiao-Dong Chen

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Li, JW., Chen, XD., Hu, XY. et al. Comparative physiological and proteomic analyses reveal different adaptive strategies by Cymbidium sinense and C. tracyanum to drought. Planta 247, 69–97 (2018). https://doi.org/10.1007/s00425-017-2768-7

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