Advertisement

Molecular Breeding

, Volume 34, Issue 3, pp 1517–1525 | Cite as

Transcriptional regulation of ABA core signaling component genes in sorghum (Sorghum bicolor L. Moench)

  • Monika Dalal
  • Madhuri Inupakutika
Short communication

Abstract

Abscisic acid (ABA) plays an important role in growth, development and adaptation of plants to environmental stresses. The mechanism of ABA signal transduction involves three core components namely ABA receptors [pyrabactin resistance 1 (PYR1)/PYR1-like (PYL)/regulatory component of ABA receptor (RCAR)], clade A PP2Cs and Class III SnRK2 family proteins. In the present study, we identified and analyzed the core components of ABA signaling in sorghum, which is known for its drought tolerance. Genome wide in silico analysis led to the identification of eight PYL ABA receptors, nine clade A PP2Cs and three class III SnRK2 family members. Abiotic stresses and exogenous ABA-mediated transcriptional changes of the genes encoding ABA core signaling components were analyzed at seedling stage. All the members of SbPYL gene family were downregulated, except SbPYL1 and SbPYL7 which showed significant upregulation in leaf under drought stress. SbPYL1 and SbPYL5 were upregulated in response to ABA, cold, high salt and PEG-induced osmotic stress, while SbPYL4 showed significant upregulation only under cold stress. Expression levels of the SbPP2C genes were higher or unaffected in response to exogenous ABA and abiotic stresses in leaf except SbPP2C5, which decreased under cold stress. SbPP2C4, SbPP2C5 and SbPP2C6 were highly induced (up to 56-fold–99-fold increase) under different stresses. Expression of class III SbSnRK2 genes was either unaffected or downregulated under abiotic stresses and exogenous ABA. Heat stress downregulated the expression of all the ABA core signaling component genes except that of SbPP2C6 which was upregulated under heat stress. In general, abiotic stresses upregulated the expression of PP2Cs but downregulated the expression of SnRK2 in sorghum seedlings. Differential stress-responsive expression and less number of PYLs in sorghum as compared with Arabidopsis suggest that SbPYL family members might have acquired distinct functions during evolution.

Keywords

ABA signaling Osmotic stress PP2C PYL SnRK2 Sorghum 

Notes

Acknowledgments

The study was funded by Indian Council of Agricultural Research, New Delhi. We thank Dr. Viswanathan Chinnusamy for critical reading of the manuscript.

Supplementary material

11032_2014_114_MOESM1_ESM.docx (562 kb)
Supplementary material 1 (DOCX 562 kb)

References

  1. Addicott FT, Lyon JL (1969) Physiology of abscisic acid and related substances. Annu Rev Plant Physiol 20:139CrossRefGoogle Scholar
  2. Boneh U, Biton I, Schwartz A, BenAri G (2012a) Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant Sci 187:89–96PubMedCrossRefGoogle Scholar
  3. Boneh U, Biton I, Zheng C, Schwartz A, BenAri G (2012b) Characterization of potential ABA receptors in Vitis vinifera. Plant Cell Rep 31:311–321PubMedCrossRefGoogle Scholar
  4. Boudsocq M, Barbier-Brygoo H, Lauriere C (2004) Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J Biol Chem 279:41758–41766PubMedCrossRefGoogle Scholar
  5. Chai YM, Jia HF, Li CL, Dong QH, Shen YY (2011) FaPYR1 is involved in strawberry fruit ripening. J Exp Bot 62:5079–5089PubMedCrossRefGoogle Scholar
  6. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679PubMedCrossRefGoogle Scholar
  7. Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485–494PubMedCrossRefPubMedCentralGoogle Scholar
  8. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signaling pathway. Nature 462:660–664PubMedCrossRefPubMedCentralGoogle Scholar
  9. He Y, Hao Q, Li W, Yan C, Yan N, Yin P (2014) Identification and characterization of ABA receptors in Oryza sativa. PLoS One 9:e95246PubMedCrossRefPubMedCentralGoogle Scholar
  10. Huai J, Wang M, He J, Zheng J, Dong Z, Lv H, Zhao J, Wang G (2008) Cloning and characterization of the SnRK2 gene family from Zea mays. Plant Cell Rep 27:1861–1868PubMedCrossRefGoogle Scholar
  11. Kim H, Hwang H, Hong JW, Lee YN, Ahn IP, Yoon IS, Yoo SD, Lee S, Lee SC, Kim BG (2012) A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. J Exp Bot 63:1013–1024PubMedCrossRefGoogle Scholar
  12. Klingler JP, Batelli G, Zhu JK (2010) ABA receptors: the START of a new paradigm in phytohormone signaling. J Exp Bot 61:3199–3210PubMedCrossRefPubMedCentralGoogle Scholar
  13. Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004) Differential activation of the rice sucrose nonfermenting1-related protein kinase 2 family by hyperosmotic stress and abscisic acid. Plant Cell 16:1163–1177PubMedCrossRefPubMedCentralGoogle Scholar
  14. Li LB, Zhang YR, Liu KC, Ni ZF, Fang ZJ, Sun QX, Gao JW (2010) Identification and bioinformatics analysis of SnRK2 and CIPK family genes in sorghum. Agric Sci China 9:19–30CrossRefGoogle Scholar
  15. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{{ - \varDelta \varDelta C_{\text{t}} }}\) method. Methods 25:402–408Google Scholar
  16. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068PubMedGoogle Scholar
  17. McCourt P, Creelman R (2008) The ABA receptors—we report you decide. Curr Opin Plant Biol 11:474–478PubMedCrossRefGoogle Scholar
  18. Melcher K, Ng LM, Zhou XE, Soon FF, Xu Y, Suino-Powell KM, Park SY, Weiner JJ, Fujii H, Chinnusamy V, Kovach A, Li J, Wang Y, Li J, Peterson FC, Jensen DR, Yong EL, Volkman BF, Cutler SR, Zhu JK, Xu HE (2009) A gate-latch lock mechanism for hormone signaling by abscisic acid receptors. Nature 462:602–608PubMedCrossRefPubMedCentralGoogle Scholar
  19. Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099PubMedCrossRefPubMedCentralGoogle Scholar
  20. Ng LM, Soon FF, Zhou XE, West GM, Kovach A, Suino-Powell KM, Chalmers MJ, Li J, Yong EL, Zhu JK, Griffin PR, Melcher K, Xu HE (2011) Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc Natl Acad Sci USA 108:21259–21264PubMedCrossRefPubMedCentralGoogle Scholar
  21. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TFF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of start proteins. Science 324:1068–1071PubMedPubMedCentralGoogle Scholar
  22. Romero P, Lafuente MT, Rodrigo MJ (2012) The Citrus ABA signalosome: identification and transcriptional regulation during sweet orange fruit ripening and leaf dehydration. J Exp Bot 63:4931–4945PubMedCrossRefPubMedCentralGoogle Scholar
  23. Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park S-Y, Marquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60:575–588PubMedCrossRefGoogle Scholar
  24. Santiago J, Dupeuxb F, Betzb K, Antonia R, Gonzalez-Guzmana M, Rodrigueza L, Marquezb JA, Rodriguez PL (2012) Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs. Plant Sci 182:3–11PubMedCrossRefGoogle Scholar
  25. Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signalling. Trends Plant Sci 9:236–243PubMedCrossRefGoogle Scholar
  26. Seiler C, Harshavardhan VT, Reddy PS, Hensel G, Kumlehn J, Eschen-Lippold L, Rajesh K, Korzun V, Wobus U, Lee J, Selvaraj G, Sreenivasulu N (2014) Abscisic acid flux alterations result in differential ABA signalling responses and impact assimilation efficiency in barley under terminal drought stress. Plant Physiol. doi: 10.1104/pp.113.229062 PubMedPubMedCentralGoogle Scholar
  27. Singh A, Giri J, Kapoor S, Tyagi AK, Pandey GK (2010) Protein phosphatase complement in rice: genome-wide identification and transcriptional analysis under abiotic stress conditions and reproductive development. BMC Genomics 11:435PubMedCrossRefPubMedCentralGoogle Scholar
  28. Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Eileen Tan MH, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong EL, Cutler SR, Zhu JK, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335:85–88PubMedCrossRefPubMedCentralGoogle Scholar
  29. Sun L, Wang YP, Chen P, Ren J, Ji K, Li Q, Li P, Dai SJ, Leng P (2011) Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress. J Exp Bot 62:5659–5669PubMedCrossRefPubMedCentralGoogle Scholar
  30. Xue T, Wang D, Zhang S, Ehlting J, Ni F, Jakab S, Zheng C, Zhong Y (2008) Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genomics 9:550PubMedCrossRefPubMedCentralGoogle Scholar
  31. Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483PubMedCrossRefGoogle Scholar
  32. Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281:5310–5318PubMedCrossRefGoogle Scholar
  33. Zhang F, Lu X, Lv Z, Zhang L, Zhu M, Jiang W, Wang G, Sun X, Tang K (2013) Overexpression of the Artemisia orthologue of ABA receptor, AaPYL9, enhances ABA sensitivity and improves artemisinin content in Artemisia annua L. PLoS One 8(2):e56697PubMedCrossRefPubMedCentralGoogle Scholar
  34. Zhao Y, Chan Z, Xing L, Liu X, Hou YJ, Chinnusamy V, Wang P, Duan C, Zhu JK (2013) The unique mode of action of a divergent member of the ABA-receptor protein family in ABA and stress signaling. Cell Res 23:1380–1395PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.National Research Centre on Plant BiotechnologyNew DelhiIndia
  2. 2.Directorate of Sorghum ResearchHyderabadIndia
  3. 3.Department of BiologyEastern New Mexico UniversityPortalesUSA

Personalised recommendations