Genome-wide identification, phylogenetic, structural and functional evolution of the core components of ABA signaling in plant species: a focus on rice.
Oryza
/ genetics
Phylogeny
Abscisic Acid
/ metabolism
Signal Transduction
/ genetics
Genome, Plant
/ genetics
Evolution, Molecular
Plant Proteins
/ genetics
Gene Expression Regulation, Plant
Gene Duplication
Stress, Physiological
/ genetics
Plant Growth Regulators
/ metabolism
Protein Phosphatase 2C
/ genetics
Arabidopsis
/ genetics
Collinearity analysis
Divergence
Evolution
Expansion
Phylogenetic analysis
Whole-genome replication
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
22 Jul 2024
22 Jul 2024
Historique:
received:
05
04
2024
accepted:
26
06
2024
medline:
23
7
2024
pubmed:
23
7
2024
entrez:
22
7
2024
Statut:
epublish
Résumé
A genome-wide analysis had identified 642 ABA core component genes from 20 plant species, which were further categorized into three distinct subfamilies. The gene structures and evolutionary relationships of these genes had been characterized. PP2C_1, PP2C_2, and SnRK2_1 had emerged as key players in mediating the ABA signaling transduction pathway, specifically in rice, in response to abiotic stresses. The plant hormone abscisic acid (ABA) is essential for growth, development, and stress response, relying on its core components, pyrabactin resistance, pyrabactin resistance-like, and the regulatory component of ABA receptor (PYR/PYL/RCAR), 2C protein phosphatase (PP2C), sucrose non-fermenting-1-related protein kinase 2 (SnRK2). However, there's a lack of research on their structural evolution and functional differentiation across plants. Our study analyzed the phylogenetic, gene structure, homology, and duplication evolution of this complex in 20 plant species. We found conserved patterns in copy number and homology across subfamilies. Segmental and tandem duplications drove the evolution of these genes, while whole-genome duplication (WGD) expanded PYR/PYL/RCAR and PP2C subfamilies, enhancing environmental adaptation. In rice and Arabidopsis, the PYR/PYL/RCAR, PP2C, and SnRK2 genes showed distinct tissue-specific expression and responded to various stresses. Notably, PP2C_1 and PP2C_2 interacted with SnRK2_1 and were crucial for ABA signaling in rice. These findings offered new insights into ABA signaling evolution, interactions, and integration in green plants, benefiting future research in agriculture, evolutionary biology, ecology, and environmental science.
Identifiants
pubmed: 39039384
doi: 10.1007/s00425-024-04475-2
pii: 10.1007/s00425-024-04475-2
doi:
Substances chimiques
Abscisic Acid
72S9A8J5GW
Plant Proteins
0
Plant Growth Regulators
0
Protein Phosphatase 2C
EC 3.1.3.16
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
58Subventions
Organisme : Sichuan Province Science and Technology Support Program
ID : 2022NSFSC0934
Organisme : the Scientific Research Foundation of Chengdu University of Information Technology
ID : KYTZ202141
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
An Y, Mi X, Xia X, Qiao D, Yu S, Zheng H, Jing T, Zhang F (2023) Genome-wide identification of the PYL gene family of tea plants (Camellia sinensis) revealed its expression profiles under different stress and tissues. BMC Genomics 24(1):362
pubmed: 37380940
pmcid: 10304716
doi: 10.1186/s12864-023-09464-5
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208
pubmed: 19458158
pmcid: 2703892
doi: 10.1093/nar/gkp335
Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Grifths-Jones S (2004) The Pfam protein families database. Nucleic Acids Res 32(suppl 1):D138–D141
pubmed: 14681378
pmcid: 308855
doi: 10.1093/nar/gkh121
Berglund AC, Sjolund E, Ostlund G (2008) InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 36:D263–D266
pubmed: 18055500
doi: 10.1093/nar/gkm1020
Boudsocq M, Droillard M, Barbier-Brygoo H, Laurière C (2007) Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol Biol 63:491–503
pubmed: 17103012
doi: 10.1007/s11103-006-9103-1
Brambilla V, Fornara F (2017) Y flowering? Regulation and activity of PYR/PYL/RCAR-domain proteins in Arabidopsis and crop species. Biochim Biophys Acta Gene Regul Mech 1860(5):655–660
pubmed: 27793713
doi: 10.1016/j.bbagrm.2016.10.009
Bulgakov VP, Wu HC, Jinn TL (2019) Coordination of ABA and chaperone signaling in plant stress responses. Trends Plant Sci 24(7):636–651
pubmed: 31085125
doi: 10.1016/j.tplants.2019.04.004
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST plus: architecture and applications. BMC Bioinform 10:421
doi: 10.1186/1471-2105-10-421
Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plant-pathogen interactions. J Plant Res 124(4):489–499
pubmed: 21380629
doi: 10.1007/s10265-011-0409-y
Chen Y, Feng L, Wei N (2017) Overexpression of cotton PYL genes in Arabidopsis enhances the transgenic plant tolerance to drought stress. Plant Physiol Biochem 115:229–238
pubmed: 28388505
doi: 10.1016/j.plaphy.2017.03.023
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: an Integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Chen K, Li GJ, Bressan RA, Song CP, Zhu JK, Zhao Y (2020b) Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62(1):25–54
pubmed: 31850654
doi: 10.1111/jipb.12899
Cheng F, Mandáková T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 25:1541–1554
pubmed: 23653472
pmcid: 3694691
doi: 10.1105/tpc.113.110486
Deng X, An B, Zhong H, Yang J, Kong W, Li Y (2019) A novel insight into functional divergence of the MST gene family in rice based on comprehensive expression patterns. Genes 10:239
pubmed: 30897847
pmcid: 6470851
doi: 10.3390/genes10030239
Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem 58:29–48
pubmed: 26374885
doi: 10.1042/bse0580029
Feng CZ, Chen Y, Wang C, Kong YH, Wu WH, Chen YF (2014) Arabidopsis RAV1 transcription factor, phosphorylated by Snrk2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80(4):654–668
pubmed: 25231920
doi: 10.1111/tpj.12670
Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N (2009) Three Snrk2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132
pubmed: 19880399
doi: 10.1093/pcp/pcp147
Garcia-Maquilon I, Coego A, Lozano-Juste J, Messerer M, de Ollas C, Julian J, Ruiz-Partida R, Pizzio G, Belda-Palazón B, Gomez-Cadenas A, Mayer KFX, Geiger D, Alquraishi SA, Alrefaei AF, Ache P, Hedrich R, Rodriguez PL (2021) PYL8 ABA receptors of Phoenix dactylifera play a crucial role in response to abiotic stress and are stabilized by ABA. J Exp Bot 72(2):757–774
pubmed: 33529339
doi: 10.1093/jxb/eraa476
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(Database issue):D1178–D1186
pubmed: 22110026
doi: 10.1093/nar/gkr944
Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12(8):343–351
pubmed: 17629540
doi: 10.1016/j.tplants.2007.06.013
Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680
pubmed: 12805596
pmcid: 167006
doi: 10.1104/pp.102.011999
Hsu PK, Dubeaux G, Takahashi Y, Schroeder JI (2021) Signaling mechanisms in abscisic acid-mediated stomatal closure. Plant J 105(2):307–321
pubmed: 33145840
doi: 10.1111/tpj.15067
Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18(9):486
pubmed: 12175810
doi: 10.1016/S0168-9525(02)02722-1
Kim S, Kang J, Cho D, Park JH, Kim SY (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40:75–87
pubmed: 15361142
doi: 10.1111/j.1365-313X.2004.02192.x
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis Version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
pubmed: 27004904
pmcid: 8210823
doi: 10.1093/molbev/msw054
Kuromori T, Seo M, Shinozaki K (2018) ABA transport and plant water stress responses. Trends Plant Sci 23(6):513–522
pubmed: 29731225
doi: 10.1016/j.tplants.2018.04.001
Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43(D1):D257–D260
pubmed: 25300481
doi: 10.1093/nar/gku949
Li N, Han X, Feng D, Yuan D, Huang LJ (2019) Signaling crosstalk between salicylic acid and ethylene/jasmonate in plant defense: do we understand what they are whispering? Int J Mol Sci 20(3):671
pubmed: 30720746
pmcid: 6387439
doi: 10.3390/ijms20030671
Li K, Ma B, Shen J, Zhao S, Ma X, Wang Z, Fan Y, Tang Q, Wei D (2021) The evolution of the expansin gene family in Brassica species. Plant Physiol Biochem 167:630–638
pubmed: 34479031
doi: 10.1016/j.plaphy.2021.08.033
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
pubmed: 11846609
doi: 10.1006/meth.2001.1262
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068
pubmed: 19407143
doi: 10.1126/science.1172408
Ma L, Yi D, Yang J, Liu X, Pang Y (2020) Genome-wide identification, expression analysis and functional study of PYR/PYL/RCAR gene family in Medicago truncatula. Plants (basel) 9(4):513
pubmed: 32316208
Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(D1):D222–D226
pubmed: 25414356
doi: 10.1093/nar/gku1221
Miyakawa T, Fujita Y, Yamguchi SK (2013) Structure and function of abscisic acid receptors. Trends Plant Sci 18(5):259–266
pubmed: 23265948
doi: 10.1016/j.tplants.2012.11.002
Nam MH, Huh SM, Kim KM, Park WJ, Seo JB, Cho K, Kim DY, Kim BG, Yoon IS (2012) Comparative proteomic analysis of early salt stress-responsive proteins in roots of Snrk2 transgenic rice. Proteome Sci 10:25
pubmed: 22462395
pmcid: 3364906
doi: 10.1186/1477-5956-10-25
Nishimura N, Sarkeshik A, Nito K, Park SY, Wang A, Carvalho PC, Lee S (2010) PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61(2):290–299
pubmed: 19874541
doi: 10.1111/j.1365-313X.2009.04054.x
Park E, Kim TH (2017) Production of ABA responses requires both the nuclear and cytoplasmic functional involvement of PYR1. Biochem Biophys Res Commun 484(1):34–39
pubmed: 28109881
doi: 10.1016/j.bbrc.2017.01.082
Park S, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071
pubmed: 19407142
pmcid: 2827199
doi: 10.1126/science.1173041
Pizzio GA, Mayordomo C, Lozano-Juste J, Garcia-Carpintero V, Vazquez-Vilar M, Nebauer SG, Kaminski KP, Ivanov NV, Estevez JC, Rivera-Moreno M, Albert A, Orzaez D, Rodriguez PL (2022) PYL1- and PYL8-like ABA receptors of Nicotiana benthamiana play a key role in ABA response in seed and vegetative tissue. Cells 11(5):795
pubmed: 35269417
pmcid: 8909036
doi: 10.3390/cells11050795
Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60:575–578
pubmed: 19624469
doi: 10.1111/j.1365-313X.2009.03981.x
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 3(11):2498–2504
doi: 10.1101/gr.1239303
Takezawa D, Komatsu K, Sakata Y (2011) ABA in bryophytes: how a universal growth regulator in life became a plant hormone? J Plant Res 124(4):437–453
pubmed: 21416316
doi: 10.1007/s10265-011-0410-5
Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform 32(5):1792–1797
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K (2009) Type 2C protein phosphatasesdirectly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad SCi USA 106:17588–17593
pubmed: 19805022
pmcid: 2754379
doi: 10.1073/pnas.0907095106
Vlad F, Rubio S, Rodrigues A, Sirichandra C, Belin C, Robert N (2009) Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21:3170–3184
pubmed: 19855047
pmcid: 2782292
doi: 10.1105/tpc.109.069179
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1040
pubmed: 21873998
doi: 10.1038/ng.919
Wang Y, Tang H, Debarry JD (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49
pubmed: 22217600
pmcid: 3326336
doi: 10.1093/nar/gkr1293
Wu JS, Lee C, Wu CC, Shiue YL (2004) Primer design using genetic algorithm. Bioinformatics 20:1710–1717
pubmed: 14988099
doi: 10.1093/bioinformatics/bth147
Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J (2002) ABA-activated Snrk2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483
pubmed: 12514244
doi: 10.1093/pcp/pcf188
Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T (2006) ABA-hypersensitive germination 3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140:115–126
pubmed: 16339800
pmcid: 1326036
doi: 10.1104/pp.105.070128
Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139
pubmed: 25104049
doi: 10.1016/j.pbi.2014.07.009
Zhang H, Mao X, Jing R (2011) SnRK2 acts within an intricate network that links sucrose metabolic and stress signaling in wheat. Plant Signal Behav 6(5):652–654
pubmed: 21448000
pmcid: 3172830
doi: 10.4161/psb.6.5.14945
Zhao H, Nie K, Zhou H, Yan X, Zhan Q, Zheng Y, Song CP (2020) ABI5 modulates seed germination via feedback regulation of the expression of the PYR/PYL/RCAR ABA receptor genes. New Phytol 228(2):596–608
pubmed: 32473058
doi: 10.1111/nph.16713