玉米遗传育种合辑Maize Genetics · Breeding · Germplasm Resources
|Functional polymorphism among members of abscisic acid receptor family (ZmPYL) in maize
LU Feng-zhong1*, YU Hao-qiang1*, LI Si1, LI Wan-chen1, ZHANG Zhi-yong2, FU Feng-ling1
1 Maize Research Institute, Sichuan Agricultural University, Chengdu 6111130, P.R.China
2 College of Life Sciences, Neijiang Normal University, Neijiang 641100, P.R.China
Pyrabactin resistance 1-like proteins (PYLs) are direct receptors of abscisic acid (ABA). For the redundant and polymorphic functions, some members of the PYL family interact with components of other signaling pathways. Here, 253 positive colonies from a maize cDNA library were screened as interacting proteins with the members of ZmPYL family. After sequencing and function annotation, 17 of 28 interaction combinations were verified by yeast two-hybrid (Y2H). The germination potential, taproot length and proline content of a quartet mutant of Arabidopsis PYL genes were significantly deceased comparing to the wild type (WT) under alkaline stress (pH 8.5) and 100 μmol L–1 methyl jasmonate (MeJA) induction. The malondialdehyde (MDA) content was significantly increased. After germinating in darkness, the characteristics of dark morphogenesis of the quartet mutant seedlings were more obvious than those of the WT. The differential expression of the related genes of photomorphogenesis in the mutant was much more than that in the WT. Three light and two JA responsive cis-affecting elements were identified during the promoter sequences of the AtPYL1 and AtPYL2 genes. These results suggested that functional polymorphism has evolved among the members of ZmPYL family. In response to developmental and environmental stimuli, they not only function as direct ABA receptors but also interact with components of other signaling pathways mediated JA, brassinosteroid (BR), auxin, etc., and even directly regulate downstream stress-related proteins. These signaling pathways can interact at various crosstalk points and different levels of gene expression within a sophisticated network.
Received: 16 April 2019
|Fund: This study was supported by the National Key Science and Technology Special Project, China (2016ZX08003-004) and the Sichuan Science and Technology Program, China (2018JY0470). We thank the technical support from the Key Laboratory of Biology and Genetic Improvement of Maize in Southwest Region, China.
Correspondence FU Feng-ling, Tel: +86-28-86290912, Fax: +86-28-86290916, E-mail: email@example.com; ZHANG Zhi-yong, Tel: +86-832-2342055, E-mail: firstname.lastname@example.org
|About author: LU Feng-zhong, E-mail: email@example.com; * These authors contributed equally to this study.
Cite this article:
LU Feng-zhong, YU Hao-qiang, LI Si, LI Wan-chen, ZHANG Zhi-yong, FU Feng-ling.
Functional polymorphism among members of abscisic acid receptor family (ZmPYL) in maize. Journal of Integrative Agriculture, 19(9): 2165-2176.
| Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell, 15, 63–78.
Aleman F, Yazaki J, Lee M, Takahashi Y, Kim A Y, Li Z, Kinoshita T, Ecker J R, Schroeder J I. 2016. An ABA-increased interaction of the PYL6 ABA receptor with MYC2 transcription factor: A putative link of ABA and JA signaling. Scientific Reports, 6, 28941.
Bai Y, Meng Y, Huang D, Qi Y, Chen M. 2011. Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics, 98, 128–136.
Bates L S, Waldron R P, Teare I D. 1973. Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205–208.
Belkhadir Y, Jaillais Y. 2015. The molecular circuitry of brassinosteroid signalling. New Phytologist, 206, 522–540.
Bhaskara G B, Nguyen T T, Verslues P E. 2012. Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiology, 160, 379–395.
Brandt B, Brodsky D E, Xue S, Negi J, Iba K, Kangasjarvi J, Ghassemian M, Stephan A B, Hu H, Schroeder J I. 2012. Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proceedings of the National Academy of Sciences of the United States of America, 109, 10593–10598.
Brandt B, Munemasa S, Wang C, Nguyen D, Yong T, Yang G P, Poretsky E, Belknap F T, Waadt R, Aleman F, Schroeder J I. 2015. Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife, 4, e03599.
Cao J, Jiang M, Li P, Chu Z. 2016. Genome-wide identification and evolutionary analysis of the PP2C gene family with their expression profiling in response to multiple stresses in Brachypodiumdistachyon. BMC Genomics, 17, 175.
Chen C W, Yang Y W, Lur H S, Tsai Y G, Chang M C. 2006. A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. The Plant Cell Physiology, 47, 1–13.
Chen J, Nolan T M, Ye H, Zhang M, Tong H, Xin P, Chu J, Chu C, Li Z, Yin Y. 2017. Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses. The Plant Cell, 29, 1425–1439.
Chini A, Boter M, Solano R. 2009. Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module. FEBS Journal, 276, 4682–4692.
Chini A, Fonseca S, Fernandez G, Adie B, Chico J M, Lorenzo O, García-Casado G, Lopez-Vidriero I, Lozano F M, Ponce M R, Micol J L, Solano R. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448, 666–671.
Clouse S D. 2011. Brassinosteroid signal transduction: From receptor kinase activation to transcriptional networks regulating plant development. The Plant Cell, 23, 1219–1230.
Cutler S R, Rodriguez P L, Finkelstein R R, Abrams S R. 2010. Abscisic acid: Emergence of a core signaling network. Annual Review of Plant Biology, 61, 651–679.
Dhindsa R S, Matowe W. 1981. Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. Journal of Experimental Botany, 32, 79–91.
de Domenico S, Bonsegna S, Horres R, Pastor V, Taurino M, Poltronieri P, Imtiaz M, Kahl G, Flors V, Winter P. 2012. Transcriptomic analysis of oxylipin biosynthesis genes and chemical profiling reveal an early induction of jasmonates in chickpea roots under drought stress. Plant Physiology & Biochemistry, 61, 115–122.
Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico J M, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla J M, Pauwels L, Witters E, Puga M I, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solanoa R. 2011. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. The Plant Cell, 23, 701–715.
Franz S, Ehlert B, Liese A, Kurth J, Cazale A C, Romeis T. 2011. Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Molecular Plant, 4, 83–96.
Friml J. 2003. Auxin transport — shaping the plant. Current Opinion in Plant Biology, 6, 7–12.
Forestan C, Meda S, Varotto S. 2010. ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm. Plant Physiology, 152, 1373–1390.
Fujji H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park S Y, Cutler S R, Sheen J, Rodriguez P L, Zhu J K. 2009. In vitro reconstitution of an abscisic acid signaling pathway. Nature, 462, 660–664.
de Gara L, Locato V, Dipierro S, de Pinto M C. 2010. Redox homeostasis in plants. The challenge of living with endogenous oxygen production. Respiratory Physiology and Neurobiology, 173, S13–S19.
Ge Y, Li Y, Zhu Y M, Bai X, Lv D K, Guo D, Ji W, Cai H. 2010. Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biology, 10, 153.
Ha Y, Shang Y, Nam K H. 2016. Brassinosteroids modulate ABA-induced stomatal closure in Arabidopsis. Journal of Experimental Botany, 67, 6297–6308.
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, e95246.
He Z H, Zhong J W, Sun X P, Wang B, Terzaghi W, Dai M. 2018. The maize ABA receptors ZmPYL8, 9, and 12 facilitate plant drought resistance. Frontiers in Plant Science, 9, 422.
Hu Y, Jiang L, Wang F, Yu D. 2013. Jasmonate regulates the inducer of CBF expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. The Plant Cell, 25, 2907–2924.
Ismail A, Riemann M, Nick P. 2012. The jasmonate pathway mediates salt tolerance in grapevines. Journal of Experimental Botany, 63, 2127–2139.
Kazan K, Manners J M. 2013. MYC2: The master in action. Molecular Plant, 6, 686–703.
Kir G, Ye H, Nelissen H, Neelakandan A K, Kusnandar A S, Luo A, Inze D, Sylvester A W, Yin Y, Becraft P W. 2015. RNA interference knockdown of BRASSINOSTEROID INSENSITIVE1 in maize reveals novel functions for brassinosteroid signaling in controlling plant architecture. Plant Physiology, 169, 826–839.
Kohli A, Sreenivasulu N, Lakshmanan P, Kumar P P. 2013. The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stress. Plant Cell Reports, 32, 945–957.
Kong X, Pan J, Zhang D, Jiang S, Cai G, Wang L, Li D. 2013. Identification of mitogen-activated protein kinase kinase gene family and MKK-MAPK interaction network in maize. Biochemical and Biophysical Research Communications, 441, 964–969.
Larkindale J, Knight M R. 2012. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology, 128, 682–695.
Li F H, Fu F L, Ni N, Sha L N, He L, Li W C. 2009. Differential expression of serine/threonine protein phosphatase type-2C under drought stress in maize. Plant Molecular Biology Reporter, 27, 29–37.
Li H, Li Y, Zhao Q, Li T, Wei J, Li B, Shen W, Yang C, Zeng Y, Rodriguez P L, Zhao Y, Jiang L, Wang X, Gao C. 2019. The plant ESCRT component FREE1 shuttles to the nucleus to attenuate abscisic acid signaling. Nature Plant, 5, 512–524.
Li J, Nagpal P, Vitart V, McMorris T C, Chory J. 1996. A role for brassinosteroids in light-dependent development of Arabidopsis. Science, 272, 398–401.
Li Y, Li Y, Liu Y, Wu Y, Xie Q. 2018. The sHSP22 heat shock protein requires the ABI1 protein phosphatase to modulate polar auxin transport and downstream responses. Plant Physiology, 176, 2406–2425.
Lin Y H, Pan K Y, Hung C H, Huang H E, Chen C L, Feng T Y, Huang L F. 2013. Overexpression of ferredoxin, PETF, enhances tolerance to heat stress in Chlamydomonas reinhardtii. International Journal of Molecular Sciences, 14, 20913–20929.
Liu S, Zhang P, Li C, Xia G. 2019. The moss jasmonate ZIM-domain protein PnJAZ1 confers salinity tolerance via crosstalk with the abscisic acid signalling pathway. Plant Science, 280, 1–11.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.
Ludwig A A, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones J D, Romeis T. 2005. Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proceedings of the National Academy of Sciences of the United States of America, 102, 10736–10741.
Ludwig-Muller J. 2011. Auxin conjugates: Their role for plant development and in the evolution of land plants. Journal of Experimental Botany, 62, 1757–1773.
Luo X M, Lin W H, Zhu S W, Zhu J Y, Sun Y, Fan X Y, Cheng M, Hao Y, Oh E, Tian M, Liu L, Zhang M, Xie Q, Chong K, Wang Z Y. 2010. Integration of light and brassinosteroid signaling pathways by a GATA transcription factor in Arabidopsis. Development Cell, 19, 872–883.
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, 1064–1068.
Miyazaki S, Koga R, Bohnert H J, Fukuhara T. 1999. Tissue- and environmental response-specific expression of 10 PP2C transcripts in Mesembryanthemum crystallinum. Molecular and General Genetics, 261, 307–316.
Momonoki Y S, Yamamoto K, Oguri S. 2009. Molecular cloning of oxygen-evolving enhancer genes induced by salt treatment in a halophyte, Salicornia europaea L. Plant Production Science, 12, 193–198.
Mou W, Li D, Luo Z, Li L, Mao L, Ying T. 2018. SlAREB1 transcriptional activation of NOR is involved in abscisic acid-modulated ethylene biosynthesis during tomato fruit ripening. Plant Science, 276, 239–249.
Oh E, Zhu J Y, Wang Z Y. 2012. Interaction between BZRl and PIF4 integrates brassinosteroid and environmental responses. Nature Cell Biology, 14, 802–809.
de Ollas C, Dodd I C. 2016. Physiological impacts of ABA-JA interactions under water-limitation. Plant Molecular Biology, 91, 641–650.
Park S Y, Fung P, Nishimura N, Jensen D R, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T F, Alfred S E, Bonetta D, Finkelstein R, Provart N J, Desveaux D, Rodriguez P L, McCourt P, Zhu J K, Schroeder J I, Volkman B F, et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, 1068–1071.
Peres A L G L, Soares J S, Tavares R G, Righetto G, Zullo M A T, Mandava N B, Menossi M. 2019. Brassinosteroids, the sixth class of phytohormones: A molecular view from the discovery to hormonal interactions in plant development and stress adaptation. International Journal of Molecular Sciences, 20, 331.
Petrasek J, Mravec J, Bouchard R, Blakeslee J J, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benková E, Perry L, Krecek P, Lee O R, Fink G R, Geisler M, Murphy A S, Luschnig C, Zazímalová E, Friml J. 2006. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science, 312, 914–918.
Pompeu G B, Vilhena M B, Gratao P L, Carvalho R F, Rossi M L, Martinelli A P, Azevedo R A. 2017. Abscisic acid-deficient sit tomato mutant responses to cadmium-induced stress. Protoplasma, 254, 771–783.
Qi T, Huang H, Wu D, Yan J, Qi Y, Song S, Xie D. 2014. Arabidopsis DELLA and JAZ proteins bind the WD-repeat/bHLH/MYB complex to modulate gibberellin and jasmonate signaling synergy. The Plant Cell, 26, 16.
Saini S, Sharma I, Pati P K. 2015. Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks. Frontiers in Plant Science, 6, 950.
Schnable P S, Ware D, Fulton R S, Stein J C, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves T A, Minx P, Reily A D, Courtney L, Kruchowski S S, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock S M. 2009. The B73 maize genome: Complexity, diversity, and dynamics. Science, 326, 1112–1115.
Seo J S, Joo J, Kim M J, Kim Y K, Nahm B H, Song S I, Cheong J J, Lee J S, Kim J K, Choi Y D. 2011. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. The Plant Journal, 65, 907–921.
Shang Y, Dai C, Lee M M, Kwak J M, Nam K H. 2016. BRI1-associated receptor kinase 1 regulates guard cell ABA signaling mediated by open stomata 1 in Arabidopsis. Molecular Plant, 9, 447–460.
Shu K, Zhou W, Chen F, Luo X, Yang W. 2018. Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Frontiers in Plant Science, 9, 416.
Siegel R S, Xue S, Murata Y, Yang Y, Nishimura N, Wang A, Schroeder J I. 2009. Calcium elevation - dependent and attenuated resting calcium - dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K+ channels in Arabidopsis guard cells. The Plant Journal, 59, 207–220.
Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altmann T, Redei G P, Nagy F, Schell J, Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell, 85, 171–182.
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He S Y, Howe G A, Browse J. 2007. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature, 448, 661–665.
Wang Y G, Fu F L, Yu H Q, Hu T, Zhang Y Y, Tao Y, Zhu J K, Zhao Y, Li W C. 2018. Interaction network of core ABA signaling components in maize. Plant Molecular Biology, 96, 245–263.
Wang Z Y, Bai M Y, Oh E, Zhu J Y. 2012. Brassinosteroid signaling network and regulation of photomorphogenesis. Annual Review of Genetics, 46, 701–724.
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frey N F D, Leung J. 2001. An update on abscisic acid signaling in plants and more. Nature, 410, 327–330.
Wild M, Daviere J M, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P. 2012. The Arabidopsis Della RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. The Plant Cell, 24, 3307–3319.
Yang Q, Liu K, Niu X, Wang Q, Wan Y, Yang F, Li G, Wang Y, Wang R. 2018. Genome-wide identification of PP2C genes and their expression profiling in response to drought and cold stresses in Medicago truncatula. Scientific Reports, 8, 12841.
Ye H, Du H, Tang N, Li X, Xiong L. 2009. Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Molecular Biology, 71, 291–305.
Yin P, Fan H, Hao Q, Yuan X, Wu D, Pang Y, Yan C, Li W, Wang J, Yan N. 2009. Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nature Structural & Molecular Biology, 16, 1230–1236.
Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J. 2005. A new class of transcription factors mediates brassinosteroid regulated gene expression in Arabidopsis. Cell, 120, 249–259.
Yu H, Feng W, Sun F, Zhang Y, Liu B, Lu F, Yang L, Fu F, Li W. 2018. Cloning and characterization of BES1/BZR1 transcription factor genes in maize. Plant Growth Regulation, 86, 235–249.
Zhang S, Cai Z, Wang X. 2009. The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proceedings of the National Academy of Sciences of the United States of America, 106, 4543–4548.
Zhao Y, Wang Y, Tang H, Wang W, Wu J, Hu X. 2016. Quantitative proteomic analyses identify ABA-related proteins and signal pathways in maize leaves under drought conditions. Frontiers in Plant Science, 7, 1827.
Zhao Y, Xing L, Wang X, Hou Y J, Gao J, Wang P, Duan C G, Zhu X, Zhu J K. 2014. The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Science Signaling, 7, ra53.
Zhao Y, Zhang Z J, Gao J H, Wang P, Hu T, Wang Z, Hou Y J, Wan Y, Liu W, Xie S, Lu T, Xue L, Liu Y, Macho A P, Tao W A, Bressan R A, Zhu J K. 2018. Arabidopsis duodecuple mutant of PYL ABA receptors reveals PYL repression of ABA independent SnRK2 activity. Cell Reports, 23, 3340–3351.
Zhou S, Wei F, Nguyen J, Bechner M, Potamousis K, Goldstein S, Pape L, Mehan M R, Churas C, Pasternak S, Forrest D K, Wise R, Ware D, Wing R A, Waterman M S, Livny M, Schwartz D C. 2009. A single molecule scaffold for the maize genome. PLoS Genetics, 5, e1000711.
Zhu D, Bai X, Chen C, Chen Q, Cai H, Li Y, Ji W, Zhai H, Lv D, Luo X, Zhu Y. 2011. GsTIFY10, a novel positive regulator of plant tolerance to bicarbonate stress and a repressor of jasmonate signaling. Plant Molecular Biology, 77, 285–297.
Zhu D, Li R T, Liu X. 2014. The positive regulatory roles of the TIFY10 proteins in plant responses to alkaline stress. PLoS ONE, 9, e111984.
Zhu J K. 2016. Abiotic stress signaling and responses in plants. Cell, 167, 313–324.
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