Cellular Mechanisms of Environmental Adaptation: Learning from Non-Arabidopsis Model Species

Chapter
Part of the Progress in Botany book series (BOTANY, volume 74)

Abstract

Soil salinity is an abiotic stressor that severely limits crop yield and agricultural productivity. Currently, comprehensive elucidations of complex networks of cellular salt adaptation provide new opportunities for the breeding and engineering of improved plant tolerance to this environmental cue. Systematic analyses of cellular pathways of salt adaptation have been particularly performed in the glycophytic model plants Arabidopsis thaliana and rice by exploiting current state-of-the-art omics methods as well as a wide range of genetic tools. Despite the wealth of knowledge provided by these studies, detailed understanding of the complex networks of cellular salt adaptation requires, however, systematic analyses of salt-adaptive mechanisms in naturally halotolerant plant species. These studies on the molecular mechanisms of salt adaptation in halophytes are very limited due to the restricted availability of genetic techniques and resources in these species. Only recently, Arabidopsis relative model species (ARMS) and rice relative model species (RRMS) have been introduced into salt stress research allowing direct comparison with the glycophytic models Arabidopsis and rice. Particularly, cross-species transcriptome analyses allowed new insights into differences of stress regulating mechanisms in glycophytes and halophytes. Here, recent discoveries on Arabidopsis and rice relative model species are reviewed focusing on regulatory systems of salt adaptation as well as their biotechnological applicability.

Keywords

Salt Stress Salt Tolerance Plant Salt Tolerance Salt Stress Response Improve Salt Tolerance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abogadallah GM (2000) Antioxidative defense under salt stress. Plant Signal Behav 5:369–374CrossRefGoogle Scholar
  2. Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol 138:171–190CrossRefGoogle Scholar
  3. Adler G, Blumwald E, Bar-Zvi D (2010) The sugar beet gene encoding the sodium/proton exchanger 1 (BvNHX1) is regulated by a MYB transcription factor. Planta 232:187–195PubMedCrossRefGoogle Scholar
  4. Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol Plant 2:3–12PubMedCrossRefGoogle Scholar
  5. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258PubMedCrossRefGoogle Scholar
  6. Arbona V, Argamasilla R, Gómez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167:1342–1350PubMedCrossRefGoogle Scholar
  7. Ashraf M, Akram NA (2009) Improving salinity tolerance of plants through conventional breeding and genetic engineering: an analytical comparison. Biotechnol Adv 27:744–752PubMedCrossRefGoogle Scholar
  8. Beffagna N, Buffoli B, Busi C (2005) Modulation of reactive oxygen species production during osmotic stress in Arabidopsis thaliana cultured cells: involvement of the plasma membrane Ca2+-ATPase and H+-ATPase. Plant Cell Physiol 46:1326–1339PubMedCrossRefGoogle Scholar
  9. Bohnert HJ, Golldack D, Ishitani M, Kamasani UR, Rammesmayer G, Shen B, Sheveleva E, Jensen RG (1999) Salt tolerance engineering—which are the essential mechanisms? In: Singhal GS, Renger G, Sopory SK, Irrgang K-D, Govindjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa Publishing House, New DelhiGoogle Scholar
  10. Chelaifa H, Mahe F, Ainouche M (2010) Transcriptome divergence between the hexaploid salt-marsh sister species Spartina maritima and Spartina alterniflora (Poaceae) Molec. Ecol 19:2050–2063Google Scholar
  11. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236PubMedCrossRefGoogle Scholar
  12. Chinnusamy V, Zhu J, Zhu JK (2006) Salt stress signaling and mechanisms of plant salt tolerance. Genet Eng (N Y) 27:141–177CrossRefGoogle Scholar
  13. Cuin TA, Bose J, Stefano G, Jha D, Tester M, Mancuso S, Shabala S (2011) Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ 34:947–961PubMedCrossRefGoogle Scholar
  14. Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507PubMedCrossRefGoogle Scholar
  15. Diédhiou CJ, Popova OV, Dietz KJ, Golldack D (2008a) The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol 8:49PubMedCrossRefGoogle Scholar
  16. Diédhiou CJ, Popova OV, Dietz KJ, Golldack D (2008b) The SUI-homologous translation initiation factor eIF-1 is involved in the regulation of ion homeostasis in rice. Plant Biol 10:298–309PubMedCrossRefGoogle Scholar
  17. Diédhiou CJ, Popova OV, Golldack D (2009a) Transcript profiling of the salt-tolerant Festuca rubra ssp. litoralis reveals a regulatory network controlling salt acclimatization. J Plant Physiol 166:697–711PubMedCrossRefGoogle Scholar
  18. Diédhiou CJ, Popova OV, Golldack D (2009b) Comparison of salt-responsive gene regulation in rice and in the salt-tolerant Festuca rubra ssp. litoralis. Plant Signal Behav 4:533–535PubMedCrossRefGoogle Scholar
  19. Dietz KJ, Tavakoli N, Kluge C, Mimura T, Sharma S, Harris GC, Chardonnens A, Golldack D (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 52:1969–1980PubMedCrossRefGoogle Scholar
  20. Fraile-Escanciano A, Kamisugi Y, Cuming AC, Rodríguez-Navarro A, Benito B (2010) The SOS1 transporter of Physcomitrella patens mediates sodium efflux in planta. New Phytol 188:750–761PubMedCrossRefGoogle Scholar
  21. Ghars MA, Parre E, Debez A, Bordenave M, Richard L, Leport L, Bouchereau A, Savouré A, Abdelly C (2008) Comparative salt tolerance analysis between Arabidopsis thaliana and Thellungiella halophila, with special emphasis on K+/Na+ selectivity and proline accumulation. J Plant Physiol 165:588–599PubMedCrossRefGoogle Scholar
  22. Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818PubMedCrossRefGoogle Scholar
  23. Golldack D (2004) Molecular responses of halophytes to high salinity. Prog Bot 65:219–234CrossRefGoogle Scholar
  24. Golldack D, Dietz KJ (2001) Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol 125:1643–1654PubMedCrossRefGoogle Scholar
  25. Golldack D, Su H, Quigley F, Kamasani UR, Muñoz-Garay C, Balderas E, Popova OV, Bennett J, Bohnert HJ, Pantoja O (2002) Characterization of a HKT-type transporter in rice as a general alkali cation transporter. Plant J 31:529–542PubMedCrossRefGoogle Scholar
  26. Golldack D, Quigley F, Michalowski CB, Kamasani UR, Bohnert HJ (2003) Salinity stress-tolerant and -sensitive rice (Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Mol Biol 51:71–81PubMedCrossRefGoogle Scholar
  27. Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391PubMedCrossRefGoogle Scholar
  28. Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839PubMedCrossRefGoogle Scholar
  29. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Phys 51:463–499CrossRefGoogle Scholar
  30. Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3:824–834PubMedCrossRefGoogle Scholar
  31. Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:660–668PubMedCrossRefGoogle Scholar
  32. Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, 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 135:1718–1737PubMedCrossRefGoogle Scholar
  33. Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413PubMedCrossRefGoogle Scholar
  34. Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5:233–238PubMedCrossRefGoogle Scholar
  35. Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. Plant Cell Environ 29:1220–1234PubMedCrossRefGoogle Scholar
  36. Kluge C, Golldack D, Dietz KJ (1999) Subunit D of the vacuolar H+-ATPase of Arabidopsis thaliana. Biochim Biophys Acta 1419:105–110PubMedCrossRefGoogle Scholar
  37. Krebs M, Beyhl D, Görlich E, Al-Rasheid KA, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci USA 107:3251–3256PubMedCrossRefGoogle Scholar
  38. Mian A, Oomen RJ, Isayenkov S, Sentenac H, Maathuis FJ, Véry AA (2011) Overexpression of a Na+ and K+ -permeable HKT transporter in barley improves salt tolerance. Plant J 68:468–479PubMedCrossRefGoogle Scholar
  39. Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45:490–495PubMedCrossRefGoogle Scholar
  40. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489PubMedCrossRefGoogle Scholar
  41. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467PubMedCrossRefGoogle Scholar
  42. Møller IS, Tester M (2007) Salinity tolerance of Arabidopsis: a good model for cereals? Trends Plant Sci 12:534–540PubMedCrossRefGoogle Scholar
  43. M'rah S, Ouerghi Z, Eymery F, Rey P, Hajji M, Grignon C, Lachaâl M (2007) Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana. J Plant Physiol 164:375–384PubMedCrossRefGoogle Scholar
  44. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663PubMedCrossRefGoogle Scholar
  45. Olías R, Eljakaoui Z, Li J, De Morales PA, Marín-Manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H + antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na + between plant organs. Plant Cell Environ 32:904–916PubMedCrossRefGoogle Scholar
  46. Orsini F, D'Urzo MP, Inan G, Serra S, Oh DH, Mickelbart MV, Consiglio F, Li X, Jeong JC, Yun DJ, Bohnert HJ, Bressan RA, Maggio A (2010) A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana. J Exp Bot 61:3787–3798PubMedCrossRefGoogle Scholar
  47. Peng H, Cheng HY, Chen C, Yu XW, Yang JN, Gao WR, Shi QH, Zhang H, Li JG, Ma H (2009) A NAC transcription factor gene of Chickpea (Cicer arietinum), CarNAC3, is involved in drought stress response and various developmental processes. J Plant Physiol 166:1934–1945PubMedCrossRefGoogle Scholar
  48. Popova OV, Golldack D (2007) In the halotolerant Lobularia maritima (Brassicaceae) salt adaptation correlates with activation of the vacuolar H+-ATPase and the vacuolar Na+/H+ antiporter. J Plant Physiol 164:1278–1288PubMedCrossRefGoogle Scholar
  49. Popova OV, Yang O, Dietz KJ, Golldack D (2008) Differential transcript regulation in Arabidopsis thaliana and the halotolerant Lobularia maritima indicates genes with potential function in plant salt adaptation. Gene 423:142–148PubMedCrossRefGoogle Scholar
  50. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767PubMedCrossRefGoogle Scholar
  51. Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146PubMedCrossRefGoogle Scholar
  52. Rice Full-Length cDNA Consortium, National Institute of Agrobiological Sciences Rice Full-Length cDNA Project Team, Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, Hotta I, Kojima K, Namiki T, Ohneda E, Yahagi W, Suzuki K, Li CJ, Ohtsuki K, Shishiki T, Foundation of Advancement of International Science Genome Sequencing & Analysis Group, Otomo Y, Murakami K, Iida Y, Sugano S, Fujimura T, Suzuki Y, Tsunoda Y, Kurosaki T, Kodama T, Masuda H, Kobayashi M, Xie Q, Lu M, Narikawa R, Sugiyama A, Mizuno K, Yokomizo S, Niikura J, Ikeda R, Ishibiki J, Kawamata M, Yoshimura A, Miura J, Kusumegi T, Oka M, Ryu R, Ueda M, Matsubara K, RIKEN, Kawai J, Carninci P, Adachi J, Aizawa K, Arakawa T, Fukuda S, Hara A, Hashizume W, Hayatsu N, Imotani K, Ishii Y, Itoh M, Kagawa I, Kondo S, Konno H, Miyazaki A, Osato N, Ota Y, Saito R, Sasaki D, Sato K, Shibata K, Shinagawa A, Shiraki T, Yoshino M, Hayashizaki Y, Yasunishi A (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301:376–379PubMedCrossRefGoogle Scholar
  53. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72PubMedGoogle Scholar
  54. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292PubMedCrossRefGoogle Scholar
  55. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901PubMedCrossRefGoogle Scholar
  56. Silva P, Gerós H (2009) Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. Plant Signal Behav 4:718–726PubMedCrossRefGoogle Scholar
  57. Sunarpi HT, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938PubMedCrossRefGoogle Scholar
  58. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709PubMedCrossRefGoogle Scholar
  59. Taji T, Komatsu K, Katori T, Kawasaki Y, Sakata Y, Tanaka S, Kobayashi M, Toyoda A, Seki M, Shinozaki K (2010) Comparative genomic analysis of 1047 completely sequenced cDNAs from an Arabidopsis-related model halophyte, Thellungiella halophila. BMC Plant Biol 10:261PubMedCrossRefGoogle Scholar
  60. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284:173–183PubMedCrossRefGoogle Scholar
  61. Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822PubMedCrossRefGoogle Scholar
  62. Urano K, Kurihara Y, Seki M, Shinozaki K (2010) ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol 13:132–138PubMedCrossRefGoogle Scholar
  63. 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 48:342–353PubMedCrossRefGoogle Scholar
  64. Volkov V, Wang B, Dominy PJ, Fricke W, Amtmann A (2003) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ 27:1–14CrossRefGoogle Scholar
  65. Wang Y, Yang C, Liu G, Jiang J (2007) Development of a cDNA microarray to identify gene expression of Puccinellia tenuiflora under saline–alkali stress. Plant Physiol Biochem 45:567–576PubMedCrossRefGoogle Scholar
  66. Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525PubMedCrossRefGoogle Scholar
  67. Wong CE, Li Y, Whitty BR, Díaz-Camino C, Akhter SR, Brandle JE, Golding GB, Weretilnyk EA, Moffatt BA, Griffith M (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol Biol 58:561–574PubMedCrossRefGoogle Scholar
  68. Xia N, Zhang G, Liu XY, Deng L, Cai GL, Zhang Y, Wang XJ, Zhao J, Huang LL, Kang ZS (2010) Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol Biol Rep 37:3703–3712PubMedCrossRefGoogle Scholar
  69. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94PubMedCrossRefGoogle Scholar
  70. Yang O, Popova OV, Süthoff U, Lüking I, Dietz KJ, Golldack D (2009) The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436:45–55PubMedCrossRefGoogle Scholar
  71. Yang R, Deng C, Ouyang B, Ye Z (2011) Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol Biol Rep 38:857–863PubMedCrossRefGoogle Scholar
  72. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229:1065–1075PubMedCrossRefGoogle Scholar
  73. Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135:615–621PubMedCrossRefGoogle Scholar
  74. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71PubMedCrossRefGoogle Scholar
  75. Zhu J, Lee BH, Dellinger M, Cui X, Zhang C, Wu S, Nothnagel EA, Zhu JK (2010) A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J 63:128–140PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Biochemistry and Physiology of Plants, Faculty of BiologyUniversity of BielefeldBielefeldGermany

Personalised recommendations