Abstract
Molecular genetics has confirmed older research and generated new insights into the ways how plants deal with adverse conditions. This body of research is now being used to interpret stress behavior of plants in new ways, and to add results from most recent genomics-based studies. The new knowledge now includes genome sequences of species that show extreme abiotic stress tolerances, which enables new strategies for applications through either molecular breeding or transgenic engineering. We will highlight some physiological features of the extremophile lifestyle, outline emerging features about halophytism based on genomics, and discuss conclusions about underlying mechanisms.
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Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol 138:171–190
Ali Z, Park HC, Ali A, Oh DH, Aman R, Kropornicka A, Hong H, Choi W, Chung WS, Kim WY, Bressan RA, Bohnert HJ, Lee SY, Yun DJ (2012) TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis-relative Thellungiella salsuginea, shows K+-specificity in the presence of NaCl. Plant Physiol 158:1463–1474
Allaby RG, Fuller DQ, Brown TA (2008) The genetic expectations of a protracted model for the origins of domesticated crops. Proc Natl Acad Sci USA 105:13982–13986
Aronson JA (1989) HALOPH: a data base of salt tolerant plants of the world. Arid land studies. University of Arizona, Tucson
Ayers RS, Westcot DW (1985) Water quality for agriculture. Fao Irrigation and Drainage Paper 29 (Rev. 1). Food and Agriculture Organization (FAO) of the United Nations. Rome
Balsamo RA, Thomson WW (1993) Ultrastructural features associated with secretion in the salt glands of Frankenia grandifolia (Frankeniaceae) and Avicennia germinans (Avicenniaceae). Am J Bot 80:1276–1283
Balsamo RA, Thomson WW (1996) Isolation of mesophyll and secretory cell protoplasts of the halophyte Ceratostigma plumbaginoides (L.): a comparison of ATPase concentration and activity. Plant Cell Rep 15:418–422
Bertorello AM, Zhu JK (2009) SIK1/SOS2 networks: decoding sodium signals via calcium-responsive protein kinase pathways. Pflugers Arch Eur J Physiol 458:613–619
Bohnert HJ, Cushman JC (2000) The ice plant cometh—models for environmental stress tolerance. J Plant Growth Regul 19:334–346
Breckle S-W (2002) Walter’s vegetation of the earth: the ecological systems of the geo-biosphere. Springer, Berlin
Bressan RA, Zhang C, Zhang H, Hasegawa PM, Bohnert HJ, Zhu JK (2001) Learning from the Arabidopsis experience. The next gene search paradigm. Plant Physiol 127:1354–1360
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, Wang X, Ott F, Müller J, Alonso-Blanco C, Borgwardt K, Schmid KJ, Weigel D (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43:956–963
Chen ZJ, Wang J, Tian L, Lee HS, Wang JJ, Chen M, Lee JJ, Josefsson C, Madlung A, Watson B, Lippman Z, Vaughn M, Pires JC, Colot V, Doerge RW, Martienssen RA, Comai L, Osborn TC (2004) The development of an Arabidopsis model system for genome-wide analysis of polyploidy effects. Biol J Linn Soc 82:689–700
Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, Fitzgerald T, Hu M, Ihm CH, Kristiansson K, Macarthur DG, Macdonald JR, Onyiah I, Pang AW, Robson S, Stirrups K, Valsesia A, Walter K, Wei J; Wellcome Trust Case Control Consortium, Tyler-Smith C, Carter NP, Lee C, Scherer SW, Hurles ME (2010) Origins and functional impact of copy number variation in the human genome. Nature 464:704–712
Cushman JC (2001) Osmoregulation in plants: implications for agriculture. Am Zool 41:758–769
Cushman JC, Bohnert HJ (1999) Crassulacean acid metabolism: molecular genetics. Annu Rev Plant Physiol Plant Mol Biol 50:305–332
Dalton FN, Maggio A, Piccinni G (2000) Simulation of shoot chloride accumulation: separation of physical and biochemical processes governing plant salt tolerance. Plant Soil 219:1–11
Dassanayake M, Oh DH, Haas J, Hernandez AG, Ali S, Hong H, Yun DJ, Bressan RA, Zhu J-K, Bohnert HJ, Cheeseman JM (2011a) The genome sequence of an extremophile Arabidopsis-relative: Thellungiella parvula. Nat Genet 43:913–918
Dassanayake M, Oh DH, Hong H, Bohnert HJ, Cheeseman JM (2011b) Importance of transcription control for halophytic life. Trends Plant Sci 16:1–3
Deng Z, Li Y, Xia R, Wang W, Huang X, Zhang L, Zhang S, Yang C, Zhang Y, Chen M, Xie Q (2009) Structural analysis of 83-kb genomic DNA from Thellungiella halophila: sequence features and micro-colinearity between salt cress and Arabidopsis thaliana. Genomics 94:324–332
Farnsworth E (2004) Hormones and shifting ecology throughout plant development. Ecology 85:5–15
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963
Flowers T, Yeo A (1995) Breeding for salinity resistance in crop plants: where next? Aust J Plant Physiol 22:875–884
Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121
Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. Q Rev Biol 61:313–337
Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K (2011) Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci 16:108–116
Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453
Freitas H, Breckle S-W (1992) Importance of bladder hairs for salt tolerance of field-grown Atriplex species from a Portuguese salt marsh. Flora 187:283–297
Glenn EP (1987) Relationship between cation accumulation and water content of salt tolerant grasses and a sedge. Plant Cell Environ 10:205–212
Glenn EP, O’Leary J (1984) Relationship between salt accumulation and water content of dicotyledonous halophytes. Plant Cell Environ 7:253–261
Glenn E, Miyamoto S, Moore D, Brown J, Thompson T, Brown P (1985) Water requirements for cultivating Salicornia bigelovii Torr. with seawater on sand in a coastal desert environment. J Arid Environ 36:711–730
Glenn E, O’Leary J, Watson M, Thompson T, Kuehl R (1991) Salicornia bigelovii Torr.: an oilseed halophyte for seawater irrigation. Science 251:1065–1067
Glenn EP, Watson MC, O’Leary JW, Axelson RD (1992) Comparison of salt tolerance and osmotic adjustment of low-sodium and high-sodium subspecies of the C4 halophyte, Atriplex canescens. Plant Cell Environ 15:711–718
Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255
Gong Q, Li P, Ma S, Rupassara SI, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839
Greenway H (1968) Growth stimulation by high chloride concentrations in halophytes. Isr J Bot 17:169–177
Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190
Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, Haberer G, Hollister JD, Ossowski S, Ottilar RP, Salamov AA, Schneeberger K, Spannagl M, Wang X, Yang L, Nasrallah ME, Bergelson J, Carrington JC, Gaut BS, Schmutz J, Mayer KF, Van de Peer Y, Grigoriev IV, Nordborg M, Weigel D, Guo YL (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476–481
Inan G, Zhang H, Li P, Wang Z, Cao Z, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737
Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115–119
Kato T, Emi M, Sato H, Arawaka S, Wada M, Kawanami T, Katagiri T, Tsuburaya K, Toyoshima I, Tanaka F, Sobue G, Matsubara K (2010) Segmental copy-number gain within the region of isopentenyl diphosphate isomerase genes in sporadic amyotrophic lateral sclerosis. Biochem Biophys Res Commun 402:438–442
Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905
Kramer PJ (1984) Problems in water relations of plants and cells. In: Kramer PJ (ed) International review of cytology, pp 254–286
Kreeb K (1974) Pflanzen an Salzstandorten. Naturwissenschaften 61:337–343
Kvitek DJ, Will JL, Gasch AP (2008) Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 4:e1000223
Le Houerou HN (1993) Salt-tolerant plants for the arid regions of the Mediterranean isoclimatic zone. In: Lieth H, Masoom A (eds) Towards the rational use of high salinity tolerant plants, vol 1. Kluwer Academic Publishers, Dordrecht, pp 403–422
Liphschitz N, Waisel Y (1982) Adaptation of plants to saline environments: salt excretion and glandular structure. In: Sen D, Rajpurohit K (eds) Tasks for vegetation science. Dr. W. Junk, The Hague, pp 197–214
Luo M, Liu X, Singh P, Cui Y, Zimmerli L, Wu K (2012) Chromatin modifications and remodeling in plant abiotic stress responses. Biochim Biophys Acta 1819:129–136
Maggio A, Zhu JK, Hasegawa PM, Bressan RA (2006) Osmogenetics: Aristotle to Arabidopsis. Plant Cell 18:1542–1557
Maggio A, Raimondi G, Martino A, De Pascale S (2007) Salt stress response in tomato beyond the salinity tolerance threshold. Environ Exp Bot 59:276–282
Mandáková T, Lysak MA (2008) Chromosomal phylogeny and karyotype evolution in x = 7 crucifer species (Brassicaceae). Plant Cell 20:2559–2570
Mata-González R, Meléndez-González R, Martínez-Hernández JJ (2001) Aerial biomass and elemental changes in Atriplex canescens and A. acanthocarpa as affected by salinity and soil water availability. USDA Forest Service Proc RMRS-P-21, pp 308-311
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Oh DH, Leidi E, Zhang Q, Hwang SM, Li Y, Quintero FJ, Jiang X, D’Urzo MP, Lee SY, Zhao Y, Bahk JD, Bressan RA, Yun DJ, Pardo JM, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222
Oh DH, Dassanayake M, Kropornika A, Paino d’Urzo M, Lambert G, Galbraith DW, Bressan RA, Zhu JK, Yun DJ, Cheeseman JM, Bohnert HJ (2010) Chromosome structures of the extreme halophyte Thellungiella parvula distinguished from Thellungiella salsuginea (T. halophila) and Arabidopsis thaliana. Plant Physiol 154:1040–1052
Ohno S (1970) Evolution by gene duplication. Springer, Berlin
Oo KS, Lang NT (2005) Developing salt tolerance in rice by mutagenesis. Omonrice 13:126–134
Orsini F, Paino D’Urzo M, Inan G, Serra S, Oh D-H, Mickelbart MV, Consiglio F, Li X, Jeong JC, Yun D-J, Bohnert HJ, Bressan RA, Maggio A (2010) Emerging new Arabidopsis-relative model systems (ARMS): a comparative study of salt tolerance parameters in eleven wild relatives of Arabidopsis thaliana. J Exp Bot 61:3787–3798
Orsini F, Accorsi M, Gianquinto G, Dinelli G, Antognoni F, Ruiz Carrasco K, Martinez E, AlNayef M, Marotti I, Bosi S, Biondi S (2011) Beyond the ionic and osmotic response to salinity in Chenopodium quinoa: functional elements of successful halophytism. Funct Plant Biol 38:818–831
Osmond CB, Bjorkman 0, Anderson DJ (1980) Physiological processes in plant ecology: towards a synthesis with Atriplex. In: Ecological studies, vol 36. Springer, New York
Popp M (1995) Salt resistance in herbaceous halophytes and mangroves. Prog Bot 56:416–429
Popp M, Albert R (1995) The role of organic solutes in salinity adaptation of mangroves and herbaceous halophytes In: Ajmal Khan M, Ungar IA (eds) Biology of salt tolerant plants. University of Karachi, Pakistan, pp 139–149
Prochnik S, Marri PR, Desany B, Rabinowicz PD, Kodira C, Mohiuddin M, Rodriguez F, Fauquet C, Tohme J, Harkins T, Rokhsar DS, Rounsley S (2012) The cassava genome: current progress, future directions. Trop Plant Biol, pp 1–7 (epub 5 January 2012)
Redondo-Gómez S, Mateos-Naranjo E, Davy AJ, Fernández-Muñoz F, Castellanos EM, Luque T, Figueroa ME (2007) Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. Ann Bot 100:555–563
Rensing SA, Lang D, Zimmer AD et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69
Rindos D (1987) The origins of agriculture: an evolutionary perspective. Academic Press, Orlando
Rodgers-Melnick E, Mane SP, Dharmawardhana P, Slavov GT, Crasta OR, Strauss SH, Brunner AM, Difazio SP (2012) Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Res 22:95–105
Sanders D (2000) Plant biology: the salty tale of Arabidopsis. Curr Biol 10:486–488
Schirmer U, Breckle S-W (1982) The role of bladders for salt removal in some Chenopodiaceae (mainly) Atriplex species. In: Sen DN, Rajpurohit KS (eds) T:VS 2 (tasks for vegetative science 2) contributions to the ecology of halophytes. Dr. W. Junk Publishers, Hague, pp 215–231
Serrano R (1996) Salt tolerance in plants and microorganisms: toxicity targets and defense responses. Int Rev Cytol 165:1–52
Swanson-Wagner RA, Eichten SR, Kumari S, Tiffin P, Stein JC, Ware D, Springer NM (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res 20:1689–1699
Tarasoft CS, Mallory-Smith CA, Ball DA (2007) Comparative plant responses of Puccinellia distans and Puccinellia nuttalliana to sodic versus normal soil types. J Arid Environ 70:403–417
Tuskan GA, Di Fazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Ungar IA, Pfeiffer CJ (1991) Ecophysiology of vascular halophytes. CRC Press, Boca Raton, p 209
Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MT, Azam S, Fan G, Whaley AM, Farmer AD, Sheridan J, Iwata A, Tuteja R, Penmetsa RV, Wu W, Upadhyaya HD, Yang SP, Shah T, Saxena KB, Michael T, McCombie WR, Yang B, Zhang G, Yang H, Wang J, Spillane C, Cook DR, May GD, Xu X, Jackson SA (2011) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30:83–89
Volkov V, Amtmann A (2006) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, has specific root ion-channel features supporting K+/Na+ homeostasis under salinity stress. Plant J 48:342–353
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139:822–835
Wang W, Wu Y, Li Y, Xie J, Zhang Z, Deng Z, Zhang Y, Yang C, Lai J, Zhang H, Bao H, Tang S, Yang C, Gao P, Xia G, Guo H, Xie Q (2010) A large insert Thellungiella halophila BIBAC library for genomics and identification of stress tolerance genes. Plant Mol Biol 72:91–99
Waszak SM, Hasin Y, Zichner T, Olender T, Keydar I, Khen M, Stütz AM, Schlattl A, Lancet D, Korbel JO (2010) Systematic inference of copy-number genotypes from personal genome sequencing data reveals extensive olfactory receptor gene content diversity. PLoS Comput Biol 6:e1000988
Waterhouse RM, Zdobnov EM, Kriventseva EV (2011) Correlating traits of gene retention, sequence divergence, duplicability and essentiality in vertebrates, arthropods, and fungi. Genome Biol Evol 3:75–86
Yang HM, Zhang JH, Zhang XY (2005) Regulation mechanisms of stomatal oscillation. J Integr Plant Biol 47:1159–1172
Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Acknowledgments
We thank Hyewon Hong (GNU, Korea) and Q. Xie (Chinese Academy of Science, Bejing, China) for permission to refer to unpublished data. This work was supported by the World Class University Program (Grant No. R32-10148), funded by the Ministry of Education, Science, and Technology, and the Next-Generation BioGreen 21 Program (Grant No. PJ008025), Rural Development Administration, Republic of Korea.
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R.A. Bressan and H.C. Park contributed equally to the article.
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Bressan, R.A., Park, H.C., Orsini, F. et al. Biotechnology for mechanisms that counteract salt stress in extremophile species: a genome-based view. Plant Biotechnol Rep 7, 27–37 (2013). https://doi.org/10.1007/s11816-012-0249-9
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DOI: https://doi.org/10.1007/s11816-012-0249-9