Journal of Plant Research

, Volume 124, Issue 4, pp 455–465 | Cite as

Origin and evolution of genes related to ABA metabolism and its signaling pathways

  • Kousuke HanadaEmail author
  • Takeshi Hase
  • Tetsuro Toyoda
  • Kazuo Shinozaki
  • Masanori Okamoto
JPR Symposium: Regular Paper Opening a New Era of ABA Research


Since plants cannot move to avoid stress, they have sophisticated acclimation mechanisms against a variety of abiotic stresses. The phytohormone abscisic acid (ABA) plays essential roles in abiotic stress tolerances in land plants. Therefore, it is interesting to address the evolutionary origins of ABA metabolism and its signaling pathways in land plants. Here, we focused on 48 ABA-related Arabidopsis thaliana genes with 11 protein functions, and generated 11 orthologous clusters of ABA-related genes from A. thaliana, Arabidopsis lyrata, Populus trichocarpa, Oryza sativa, Selaginella moellendorffii, and Physcomitrella patens. Phylogenetic analyses suggested that the common ancestor of these six species possessed most of the key protein functions of ABA-related genes. In two species (A. thaliana and O. sativa), duplicate genes related to ABA signaling pathways contribute to the expression variation in different organs or stress responses. In particular, there is significant expansion of gene families related to ABA in evolutionary periods associated with morphological divergence. Taken together, these results suggest that expansion of the gene families related to ABA signaling pathways may have contributed to the sophisticated stress tolerance mechanisms of higher land plants.


Abscisic acid (ABA) Arabidopsis thaliana Duplication Expression divergence Functionalization Plant evolution 



This work was supported by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN to K.H.), Grants-in-Aid for Scientific Research (to K.H.), and a research fellowship from the Japan Society for the Promotion of Science for Young Scientists (to M.O.).

Supplementary material

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  1. Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Chen K, Durand D, Farach-Colton M (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 7:429–447PubMedCrossRefGoogle Scholar
  4. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743PubMedCrossRefGoogle Scholar
  5. Cutler SC, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679PubMedCrossRefGoogle Scholar
  6. DeLong A, Calderon-Urrea A, Dellaporta SL (1993) Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74:757–768PubMedCrossRefGoogle Scholar
  7. Dongen SV (2000) Graph clustering by flow simulation. PhD thesis, University of UtrechtGoogle Scholar
  8. Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166Google Scholar
  9. Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45PubMedGoogle Scholar
  10. Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415PubMedCrossRefGoogle Scholar
  11. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedGoogle Scholar
  12. Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385PubMedCrossRefGoogle Scholar
  13. 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 signalling pathway. Nature 462:660–664PubMedCrossRefGoogle Scholar
  14. Ganko EW, Meyers BC, Vision TJ (2007) Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 24:2298–2309PubMedCrossRefGoogle Scholar
  15. Gu Z, Nicolae D, Lu HH, Li WH (2002) Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Genet 18:609–613PubMedCrossRefGoogle Scholar
  16. Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148:993–1003PubMedCrossRefGoogle Scholar
  17. Hanada K, Kuromori T, Myouga F, Toyoda T, Li WH, Shinozaki K (2009a) Evolutionary persistence of functional compensation by duplicate genes in Arabidopsis. Genome Biol Evol 1:409–414PubMedCrossRefGoogle Scholar
  18. Hanada K, Kuromori T, Myouga F, Toyoda T, Shinozaki K (2009b) Increased expression and protein divergence in duplicate genes is associated with morphological diversification. PLoS Genet 5:e1000781PubMedCrossRefGoogle Scholar
  19. Hayashi K, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, Hanada A, Nakashima T, Nakajima M, Mander LN, Yamane H, Hasebe M, Nozaki H (2010) Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol 153:1085–1097PubMedCrossRefGoogle Scholar
  20. He X, Zhang J (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164PubMedCrossRefGoogle Scholar
  21. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H, Tanahashi T, Hasebe M, Banks JA, Ashikari M, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2007) The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens. Plant Cell 19:3058–3079PubMedCrossRefGoogle Scholar
  22. Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution 61:995–1016PubMedCrossRefGoogle Scholar
  23. Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708PubMedCrossRefGoogle Scholar
  24. Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107:2355–2360PubMedCrossRefGoogle Scholar
  25. Knight CD, Sehgal A, Atwal K, Wallace JC, Cove DJ, Coates D, Quatrano RS, Bahadur S, Stockley PG, Cuming AC (1995) Molecular responses to abscisic-acid and stress are conserved between moss and cereals. Plant Cell 7:499–506PubMedCrossRefGoogle Scholar
  26. Komatsu K, Nishikawa Y, Ohtsuka T, Taji T, Quatrano RS, Tanaka S, Sakata Y (2009) Functional analyses of the ABI1-related protein phosphatase type 2C reveal evolutionarily conserved regulation of abscisic acid signaling between Arabidopsis and the moss Physcomitrella patens. Plant Mol Biol 70:327–340PubMedCrossRefGoogle Scholar
  27. Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA 107:2361–2366PubMedCrossRefGoogle Scholar
  28. Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656PubMedCrossRefGoogle Scholar
  29. Marella HH, Sakata Y, Quatrano RS (2006) Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3-like genes from Physcomitrella patens. Plant J 46:1032–1044PubMedCrossRefGoogle Scholar
  30. Milborrow B, Burden R, Taylor H (1997) The conversion of 2-cis-[C-14]xanthoxic acid into [C-14]ABA. Phytochemistry 45:257–260CrossRefGoogle Scholar
  31. Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363PubMedCrossRefGoogle Scholar
  32. Nambara E, Marion-Poll A (2003) ABA action and interactions in seeds. Trends Plant Sci 8:213–217PubMedCrossRefGoogle Scholar
  33. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185PubMedCrossRefGoogle Scholar
  34. Ohno S (1970) Evolution by gene duplication. Springer, New YorkGoogle Scholar
  35. Parry A, Neill S, Horgan R (1988) Xanthoxin levels and metabolism in the wild-type and wilty mutants of tomato. Planta 173:397–404CrossRefGoogle Scholar
  36. Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401PubMedCrossRefGoogle Scholar
  37. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  38. Sakata Y, Komatsu K, Taji T, Tanaka S (2009) Role of PP2C-mediated ABA signaling in the moss Physcomitrella patens. Plant Signal Behav 4:887–889PubMedCrossRefGoogle Scholar
  39. Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48PubMedCrossRefGoogle Scholar
  40. Seo M, Aoki H, Koiwai H, Kamiya Y, Nambara E, Koshiba T (2004) Comparative studies on the Arabidopsis aldehyde oxidase (AAO) gene family revealed a major role of AAO3 in ABA biosynthesis in seeds. Plant Cell Physiol 45:1694–1703PubMedCrossRefGoogle Scholar
  41. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  42. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  43. Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106:17588–17593PubMedCrossRefGoogle Scholar
  44. Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2006) ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140:115–126PubMedCrossRefGoogle Scholar
  45. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685PubMedCrossRefGoogle Scholar
  46. Zhang J, Rosenberg HF, Nei M (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95:3708–3713PubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2011

Authors and Affiliations

  • Kousuke Hanada
    • 1
    • 2
    • 3
    Email author
  • Takeshi Hase
    • 1
  • Tetsuro Toyoda
    • 2
  • Kazuo Shinozaki
    • 1
  • Masanori Okamoto
    • 4
    • 5
  1. 1.Gene Discovery Research GroupRIKEN Plant Science CenterYokohamaJapan
  2. 2.Bioinformatics and Systems Engineering DivisionRIKENYokohamaJapan
  3. 3.Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  4. 4.Institute of Plant Science and ResourcesOkayama UniversityKurashikiJapan
  5. 5.Center for Plant Cell Biology, Department of Botany and Plant SciencesUniversity of California, RiversideRiversideUSA

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