Protein Phosphorylation and Its Regulatory Roles in Seed Dormancy and Germination

doi:10.11983/CBB21011

Abstract

Abstract: Seed dormancy and germination are two distinct but closely related physiological processes, which are also key stages during plant life-cycle and have great significance to agricultural production, plant species reproduction, and geographical distribution. These processes are precisely regulated by interactions between different endogenous phytohormones and environmental signals. A large number of studies have shown that protein phosphorylation, plays an important role in regulating seed dormancy and germination, as well as plant response to stresses. This review paper briefly introduces the procedures and functions of protein phosphorylation and dephosphorylation modification, and summarizes the regulatory roles of protein phosphorylation modification in seed dormancy and germination. Finally, some future research directions are prospected.

Key words: seed, dormancy, germination, protein phosphorylation, phytohormone

Xiaoting Zhao, Kaitao Mao, Jiahui Xu, Chuan Zheng, Xiaofeng Luo, Kai Shu. Protein Phosphorylation and Its Regulatory Roles in Seed Dormancy and Germination[J]. Chinese Bulletin of Botany, 2021, 56(4): 488-499.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.chinbullbotany.com/EN/10.11983/CBB21011

https://www.chinbullbotany.com/EN/Y2021/V56/I4/488

Figures/Tables 1

References 102

[1]	翁华, 冉亮, 魏群 (2003). 植物蛋白磷酸酶及其在植物抗逆中的作用. 植物学通报 20, 609-615.
[2]	杨立文, 刘双荣, 林荣呈 (2019). 光信号与激素调控种子休眠和萌发研究进展. 植物学报 54, 569-581. DOI
[3]	张静, 侯岁稳 (2019). 蛋白质翻译后修饰在ABA信号转导中的作用. 植物学报 54, 300-315. DOI
[4]	朱丹, 曹汉威, 李媛, 任东涛 (2020). 植物蛋白磷酸化的检测方法. 植物学报 55, 76-82. DOI
[5]	Antoni R, Gonzalez-Guzman M, Rodriguez L, Rodrigues A, Pizzio GA, Rodriguez PL (2012). Selective inhibition of clade a phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiol 158, 970-980. DOI URL
[6]	Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F (2009). Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol 150, 1006-1021. DOI PMID
[7]	Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006). Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci USA 103, 17042-17047. DOI URL
[8]	Bewley JD (1997). Seed germination and dormancy. Plant Cell 9, 1055-1066.
[9]	Biddulph TB, Plummer JA, Setter TL, Mares DJ (2007). Influence of high temperature and terminal moisture stress on dormancy in wheat (Triticum aestivum L.). Field Crop Res 103, 139-153. DOI URL
[10]	Bigeard J, Rayapuram N, Pflieger D, Hirt H (2014). Phosphorylation-dependent regulation of plant chromatin and chromatin-associated proteins. Proteomics 14, 2127-2140. DOI PMID
[11]	Bodrone MP, Rodríguez MV, Arisnabarreta S, Batlla D (2017). Maternal environment and dormancy in sunflower: the effect of temperature during fruit development. Eur J Agron 82, 93-103. DOI URL
[12]	Boudsocq M, Barbier-Brygoo H, Laurière 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, 41758-41766. PMID
[13]	Breeze E (2019). Letting sleeping DOGs lie: regulation of DOG1 during seed dormancy. Plant Cell 31, 1218-1219. DOI
[14]	Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ (2008). Seed after- ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J 53, 214-224. PMID
[15]	Chen F, Zhou WG, Yin H, Luo XF, Chen W, Liu X, Wang XC, Meng YJ, Feng LY, Qin YY, Zhang CY, Yang F, Yong TW, Wang XC, Liu J, Du JB, Liu WG, Yang WY, Shu K (2020). Shading of the mother plant during seed development promotes subsequent seed germination in soybean. J Exp Bot 71, 2072-2084. DOI PMID
[16]	Cheng SH, Willmann MR, Chen HC, Sheen J (2002). Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129, 469-485.
[17]	Cheng XY, Wu Y, Guo JP, Du B, Chen RZ, Zhu LL, He GC (2013). A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J 76, 687-698. DOI URL
[18]	Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005). Arabidopsis calcium- dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139, 1750-1761. DOI URL
[19]	Colcombet J, Hirt H (2008). Arabidopsis MAPKs: a complex signaling network involved in multiple biological processes. Biochem J 413, 217-226. DOI PMID
[20]	Cyrek M, Fedak H, Ciesielski A, Guo YW, Sliwa A, Brzezniak L, Krzyczmonik K, Pietras Z, Kaczanowski S, Liu FQ, Swiezewski S (2016). Seed dormancy in Arabidopsis is controlled by alternative polyadenylation of DOG1. Plant Physiol 170, 947-955. DOI URL
[21]	Finch-Savage WE, Leubner-Metzger G (2006). Seed dormancy and the control of germination. New Phytol 171, 501-523. PMID
[22]	Finkelstein R, Reeves W, Ariizumi T, Steber C (2008). Molecular aspects of seed dormancy. Annu Rev Plant Biol 59, 387-415. DOI PMID
[23]	Finkelstein RR, Gampala SSL, Rock CD (2002). Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl), S15-S45. DOI URL
[24]	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, 485-494. DOI URL
[25]	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, 8380-8385. DOI URL
[26]	Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (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. DOI URL
[27]	Gong X, Li CD, Zhou MX, Bonnardeaux Y, Yan GJ (2014). Seed dormancy in barley is dictated by genetics, environments and their interactions. Euphytica 197, 355-368. DOI URL
[28]	González-García MP, Rodríguez D, Nicolás C, Rodríguez PL, Nicolás G, Lorenzo O (2003). Negative regulation of abscisic acid signaling by the Fagus sylvatica FsPP2C1 plays a role in seed dormancy regulation and promotion of seed germination. Plant Physiol 133, 135-144. PMID
[29]	Gu XY, Kianian SF, Foley ME (2006). Dormancy genes from weedy rice respond divergently to seed development environments. Genetics 172, 1199-1211. DOI URL
[30]	Guan CM, Wang XC, Feng J, Hong SL, Liang Y, Ren B, Zuo JR (2014). Cytokinin antagonizes abscisic acid- mediated inhibition of cotyledon greening by promoting the degradation of ABSCISIC ACID INSENSITIVE5 protein in Arabidopsis. Plant Physiol 164, 1515-1526. DOI URL
[31]	Gubler F, Millar AA, Jacobsen JV (2005). Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol 8, 183-187. PMID
[32]	Hanks SK, Hunter T (1995). The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9, 576-596. PMID
[33]	Hepler PK (2005). Calcium: a central regulator of plant growth and development. Plant Cell 17, 2142-2155. PMID
[34]	Hong SW, Jon JH, Kwak JM, Nam HG (1997). Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt, and cold treatments in Arabidopsis thaliana. Plant Physiol 113, 1203-1212. PMID
[35]	Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003). The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132, 666-680. DOI URL
[36]	Humphrey SJ, James DE, Mann M (2015). Protein phosphorylation: a major switch mechanism for metabolic regulation. Trends Endocrinol Metab 26, 676-687. DOI URL
[37]	Jha SK, Malik S, Sharma M, Pandey A, Pandey GK (2017). Recent advances in substrate identification of protein kinases in plants and their role in stress management. Curr Genomics 18, 523-541.
[38]	Katagiri T, Ishiyama K, Kato T, Tabata S, Kobayashi M, Shinozaki K (2005). An important role of phosphatidic acid in ABA signaling during germination in Arabidopsis thaliana. Plant J 43, 107-117. PMID
[39]	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, 1013-1024. DOI URL
[40]	Kim W, Lee Y, Park J, Lee N, Choi G (2013). HONSU, a protein phosphatase 2C, regulates seed dormancy by inhibiting ABA signaling in Arabidopsis. Plant Cell Physiol 54, 555-572. DOI URL
[41]	Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004). Differential activation of the rice sucrose nonfermenting 1-related protein kinase 2 family by hyperosmotic stress and abscisic acid. Plant Cell 16, 1163-1177. PMID
[42]	Lee SJ, Lee MH, Kim JI, Kim SY (2015). Arabidopsis putative MAP kinase kinase kinases Raf10 and Raf11 are positive regulators of seed dormancy and ABA response. Plant Cell Physiol 56, 84-97. DOI URL
[43]	Li XY, Kong XG, Huang Q, Zhang Q, Ge H, Zhang L, Li GM, Peng L, Liu ZB, Wang JM, Li XF, Yang Y (2019). CARK1 phosphorylates subfamily III members of ABA receptors. J Exp Bot 70, 519-528. DOI URL
[44]	Liu J, Hasanuzzaman M, Wen HL, Zhang J, Peng T, Sun HW, Zhao QZ (2019). High temperature and drought stress cause abscisic acid and reactive oxygen species accumulation and suppress seed germination growth in rice. Protoplasma 256, 1217-1227. DOI URL
[45]	Lorenzo O, Rodríguez D, Nicolás G, Rodríguez PL, Nicolás C (2001). A new protein phosphatase 2C (FsPP2C1) induced by abscisic acid is specifically expressed in dormant beechnut seeds. Plant Physiol 125, 1949-1956. PMID
[46]	Luan S (2003). Protein phosphatases in plants. Annu Rev Plant Biol 54, 63-92 DOI URL
[47]	Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002). Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14(Suppl), S389-S400. DOI URL
[48]	Luo XF, Dai YJ, Zheng C, Yang YZ, Chen W, Wang QC, Chandrasekaran U, Du JB, Liu WG, Shu K (2021). The ABI4-RbohD/VTC2 regulatory module promotes reactive oxygen species (ROS) accumulation to decrease seed germination under salinity stress. New Phytol 229, 950-962. DOI URL
[49]	Martinez SA, Shorinola O, Conselman S, See D, Skinner DZ, Uauy C, Steber CM (2020). Exome sequencing of bulked segregants identified a novel TaMKK3-A allele linked to the wheat ERA8 ABA-hypersensitive germination phenotype. Theor Appl Genet 133, 719-736. DOI PMID
[50]	Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001). The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signaling pathway. Plant J 25, 295-303. PMID
[51]	Nakabayashi K, Bartsch M, Xiang Y, Miatton E, Pellengahr S, Yano R, Seo M, Soppe WJJ (2012). The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION 1 protein levels in freshly harvested seeds. Plant Cell 24, 2826-2838. DOI URL
[52]	Nakagami H, Pitzschke A, Hirt H (2005). Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10, 339-346. DOI URL
[53]	Nakamura S, Pourkheirandish M, Morishige H, Kubo Y, Nakamura M, Ichimura K, Seo S, Kanamori H, Wu JZ, Ando T, Hensel G, Sameri M, Stein N, Sato K, Matsumoto T, Yano M, Komatsuda T (2016). Mitogen-activated protein kinase kinase 3 regulates seed dormancy in barley. Curr Biol 26, 775-781. DOI PMID
[54]	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, 1345-1363. DOI PMID
[55]	Née G, Kramer K, Nakabayashi K, Yuan BJ, Xiang Y, Miatton E, Finkemeier I, Soppe WJJ (2017). DELAY OF GERMINATION 1 requires PP2C phosphatases of the ABA signaling pathway to control seed dormancy. Nat Commun 8, 72. DOI URL
[56]	Nguyen QTC, Lee SJ, Choi SW, Na YJ, Song MR, Hoang QTN, Sim SY, Kim MS, Kim JI, Soh MS, Kim SY (2019). Arabidopsis Raf-like kinase Raf10 is a regulatory component of core ABA signaling. Mol Cells 42, 646-660. DOI PMID
[57]	Nishimura N, Tsuchiya W, Moresco JJ, Hayashi Y, Satoh K, Kaiwa N, Irisa T, Kinoshita T, Schroeder JI, Yates JR III, Hirayama T, Yamazaki T (2018). Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nat Commun 9, 2132. DOI PMID
[58]	Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T (2007). ABA-Hypersensitive Germination 1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J 50, 935-949. PMID
[59]	Nonogaki H (2017). Seed biology updates-highlights and new discoveries in seed dormancy and germination research. Front Plant Sci 8, 524.
[60]	Nonogaki H, Bassel GW, Bewley JD (2010). Germination-still a mystery. Plant Sci 179, 574-581. DOI URL
[61]	Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006). Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648. DOI URL
[62]	Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K (2005). Leucine-rich repeat receptor-like kinase 1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17, 1105-1119. PMID
[63]	Pelagio-Flores R, Muñoz-Parra E, Barrera-Ortiz S, Ortiz- Castro R, Saenz-Mata J, Ortega-Amaro MA, Jiménez- Bremont JF, López-Bucio J (2019). The cysteine-rich receptor-like protein kinase CRK28 modulates Arabidopsis growth and development and influences abscisic acid responses. Planta 251, 2. DOI PMID
[64]	Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010). ABA perception and signaling. Trends Plant Sci 15, 395-401. DOI PMID
[65]	Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012). Seed germination and vigor. Annu Rev Plant Biol 63, 507-533. DOI PMID
[66]	Resentini F, Felipo-Benavent A, Colombo L, Blázquez MA, Alabadí D, Masiero S (2015). TCP14 and TCP15 mediate the promotion of seed germination by gibberellins in Arabidopsis thaliana. Mol Plant 8, 482-485. DOI URL
[67]	Rubio S, Rodrigues A, Saez A, Dizon MB, Galle A, Kim TH, Santiago J, Flexas J, Schroeder JI, Rodriguez PL (2009). Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150, 1345-1355. DOI URL
[68]	Saavedra X, Modrego A, Rodríguez D, González-García MP, Sanz L, Nicolás G, Lorenzo O (2010). The nuclear interactor PYL8/RCAR3 of Fagus sylvatica FsPP2C1 is a positive regulator of abscisic acid signaling in seeds and stress. Plant Physiol 152, 133-150. DOI PMID
[69]	Schwartz PA, Murray BW (2011). Protein kinase biochemistry and drug discovery. Bioorg Chem 39, 192-210. DOI PMID
[70]	Schweighofer A, Meskiene I (2015). Phosphatases in plants. In: Schulze W, eds. Plant Phosphoproteomics. Methods in Molecular Biology, Vol 1306. New York: Humana Press. pp. 25-46.
[71]	Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y, North H, Marion-Poll A, Sun TP, Koshiba T, Kamiya Y, Yamaguchi S, Nambara E (2006). Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48, 354-366. DOI URL
[72]	Seo M, Nambara E, Choi G, Yamaguchi S (2009). Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69, 463-472. DOI URL
[73]	Shen K, Hines AC, Schwarzer D, Pickin KA, Cole PA (2005). Protein kinase structure and function analysis with chemical tools. Biochim Biophys Acta 1754, 65-78. PMID
[74]	Shiu SH, Bleecker AB (2001a). Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98, 10763-10768. DOI URL
[75]	Shiu SH, Bleecker AB (2001b). Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE (113), re22.
[76]	Shiu SH, Bleecker AB (2003). Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132, 530-543. DOI URL
[77]	Shu K, Liu XD, Xie Q, He ZH (2016). Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9, 34-45. DOI URL
[78]	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, 435. DOI URL
[79]	Tatematsu K, Nakabayashi K, Kamiya Y, Nambara E (2008). Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. Plant J 53, 42-52. PMID
[80]	Torada A, Koike M, Ogawa T, Takenouchi Y, Tadamura K, Wu JZ, Matsumoto T, Kawaura K, Ogihara Y (2016). A causal gene for seed dormancy on wheat chromosome 4A encodes a MAP kinase kinase. Curr Biol 26, 782-787. DOI URL
[81]	Uhrig RG, Labandera AM, Tang LY, Sieben NA, Goudreault M, Yeung E, Gingras AC, Samuel MA, Moorhead GBG (2017). Activation of mitochondrial protein phosphatase SLP2 by MIA40 regulates seed germination. Plant Physiol 173, 956-969. DOI PMID
[82]	Viswanathan C, Zhu JK (2002). Molecular genetic analysis of cold-regulated gene transcription. Philos Trans R Soc Lond B Biol Sci 357, 877-886. DOI URL
[83]	Walker JC (1993). Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J 3, 451-456. PMID
[84]	Walker JC, Zhang R (1990). Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345, 743-746. DOI URL
[85]	Wang JL, Zhang Q, Yu Q, Peng L, Wang JM, Dai QL, Yang Y, Li XY (2019). CARK6 is involved in abscisic acid to regulate stress responses in Arabidopsis thaliana. Biochem Biophys Res Commun 513, 460-464. DOI URL
[86]	Wang WQ, Ye JQ, Rogowska-Wrzesinska A, Wojdyla KI, Jensen ON, Møller IM, Song SQ (2014). Proteomic comparison between maturation drying and prematurely imposed drying of Zea mays seeds reveals a potential role of maturation drying in preparing proteins for seed germination, seedling vigor, and pathogen resistance. J Proteome Res 13, 606-626. DOI URL
[87]	Wu Z, Liang S, Song W, Lin GZ, Wang WG, Zhang HQ, Han ZF, Chai JJ (2017). Functional and structural characterization of a receptor-like kinase involved in germination and cell expansion in Arabidopsis. Front Plant Sci 8, 1999. DOI URL
[88]	Xiang Y, Nakabayashi K, Ding J, He F, Bentsink L, Soppe WJJ (2014). Reduced Dormancy 5 encodes a protein phosphatase 2C that is required for seed dormancy in Arabidopsis. Plant Cell 26, 4362-4375. DOI URL
[89]	Xiang Y, Song BX, Nee G, Kramer K, Finkemeier I, Soppe WJJ (2016). Sequence polymorphisms at the REDUCED DORMANCY 5 pseudophosphatase underlie natural variation in Arabidopsis dormancy. Plant Physiol 171, 2659-2670. DOI PMID
[90]	Xing Y, Jia WS, Zhang JH (2009). AtMKK1 and AtMPK6 are involved in abscisic acid and sugar signaling in Arabidopsis seed germination. Plant Mol Biol 70, 725-736. DOI PMID
[91]	Xiong LM, Lee BH, Ishitani M, Lee H, Zhang CQ, Zhu JK (2001). FIERY1 encoding an inositol polyphosphate 1- phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Gene Dev 15, 1971-1984. PMID
[92]	Xu R, Duan PG, Yu HY, Zhou ZK, Zhang BL, Wang RC, Li J, Zhang GZ, Zhuang SS, Lyu J, Li N, Chai TY, Tian ZX, Yao SG, Li YH (2018). Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol Plant 11, 860-873. DOI URL
[93]	Ye YY, Ding YF, Jiang Q, Wang FJ, Sun JW, Zhu C (2017). The role of receptor-like protein kinases (RLKs) in abiotic stress response in plants. Plant Cell Rep 36, 235-242. DOI URL
[94]	Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2006). ABA-Hyper- sensitive 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. PMID
[95]	Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006). Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140, 558-579. DOI URL
[96]	Yu XF, Han JP, Li L, Zhang Q, Yang GX, He GY (2020). Wheat PP2C-a10 regulates seed germination and drought tolerance in transgenic Arabidopsis. Plant Cell Rep 39, 635-651. DOI URL
[97]	Zhang L, Li XY, Li DK, Sun YN, Li Y, Luo Q, Liu ZB, Wang JM, Li XF, Zhang H, Lou ZY, Yang Y (2018). CARK1 mediates ABA signaling by phosphorylation of ABA receptors. Cell Discov 4, 30. DOI URL
[98]	Zhang W, Cochet F, Ponnaiah M, Lebreton S, Matheron L, Pionneau C, Boudsocq M, Resentini F, Huguet S, Blázquez MÁ, Bailly C, Puyaubert J, Baudouin E (2019). The MPK8-TCP14 pathway promotes seed germination in Arabidopsis. Plant J 100, 677-692. DOI
[99]	Zhang XJ, Yang GY, Shi R, Han XM, Qi LW, Wang RG, Xiong LM, Li GJ (2013). Arabidopsis cysteine-rich receptor-like kinase 45 functions in the responses to abscisic acid and abiotic stresses. Plant Physiol Biochem 67, 189-198. DOI URL
[100]	Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP (2011a). The Arabidopsis Ca²⁺-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192, 61-73. DOI PMID
[101]	Zhao R, Wang XF, Zhang DP (2011b). CPK12: a Ca²⁺- dependent protein kinase balancer in abscisic acid signaling. Plant Signal Behav 6, 1687-1690. DOI PMID
[102]	Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007). Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19, 3019-3036. DOI URL

酶	大类	关键基因	分子功能	参考文献
蛋白激酶	MAPKs	MPK8	通过与GA反应的转录因子TCP14相互作用磷酸化TCP14, 增强其转录活性, 调控从休眠到萌发的转换。	Zhang et al., 2019
		MKK1、 MPK6	参与ABA和糖调节的种子萌发, 通过增强ABA的合成与信号强度, 维持种子休眠, 抑制种子萌发。	Xing et al., 2009
		Raf10、 Raf11	过表达Raf10和Raf11, 使种子对ABA敏感性增强, ABI3和ABI5表达上调, 从而延缓种子萌发。	Lee et al., 2015
		MKK3	MKK3-A高表达促进小麦种子休眠释放, 且MKK3可以与Qsd2-AK相互作用, 调控大麦种子休眠。	Nakamura et al., 2016; Torada et al., 2016
	CPKs	CPK4、 CPK11	过表达CPK4和CPK11, 种子表现出对ABA敏感表型, 萌发受到明显抑制。	Zhu et al., 2007
		CPK12	CPK12通过与ABI2相互作用磷酸化ABI2, 并下调ABF1和ABF4表达, 负调控ABA信号, 促进种子萌发。	Zhao et al., 2011a, 2011b
		CPK32	CPK32通过与ABF4相互作用磷酸化ABF4, 增强其转录活性, 促进ABA信号转导, 抑制种子萌发。	Choi et al., 2005
	SnRKs	SnRK2.2、 SnRK2.3	ABA信号通路复合物PYLs-ABA-PP2C通过激活SnRK2.2和SnRK2.3激酶活性, 激活下游转录因子, 诱导种子对ABA的响应。	Finkelstein et al., 2008; Fujii and Zhu, 2009
		SAPK2	ABA受体PYL/RCAR5作用于SAPK2上游, 激活SAPK2激酶活性, 通过OREB1介导ABA信号转导, 激活ABRE启动子活性, 负调控种子萌发。	Kim et al., 2012
类受体激酶	RLKs	GRACE	编码膜蛋白, 在干种子中高表达, 其表达水平受ABA诱导, 进而延缓种子萌发, 维持种子休眠。	Wu et al., 2017
		RPK1	RPK1基因表达受ABA诱导, 通过正调控ABA信号传导, 抑制种子萌发。	Hong et al., 1997; Osakabe et al., 2005
		CRK28	CRK28能够上调ABI3和ABI5的表达, 使ABA反应增强, 削弱种子萌发。	Pelagio-Flores et al., 2019
		CRK45	过表达CRK45能够上调ABA合成及反应基因表达水平, 正调控ABA信号转导, 延缓种子萌发。	Zhang et al., 2013
		CARK1、 CARK6	CARK1和CARK6通过与ABA受体RCAR11-14相互作用, 使其磷酸化, 促进ABA信号转导, 最终抑制种子萌发。	Zhang et al., 2018; Wang et al., 2019
		OsLecRK	OsLecRK表达受萌发信号刺激而上调, 进而与OsADF相互作用, 并进一步转导萌发信号, 上调α-淀粉酶基因表达, 增强种子活力, 促进种子萌发。	Cheng et al., 2013
磷酸酶	PP2Cs	AHG1、 AHG3	DOG1与AHG1/AHG3相互作用, 形成PP2C磷酸酶复合物, 抑制其磷酸酶活性, 进而增强ABA信号, 促使种子休眠。	Née et al., 2017; Nishimura et al., 2018
		PP2C-a10	PP2C-a10与TaDOG1L1和TaDOG1L4互作, 促进小麦种子萌发; 也可与ABA反应基因(ABI3、ABI4、ABI5、EM1和EM6)互作, 降低其表达水平, 促进拟南芥种子萌发。	Yu et al., 2020
		ABI1、 ABI2	在ABA存在条件下, ABA与PYR1/PYL/RCAR受体结合, 抑制ABI1和ABI2活性, 激活SnRK2s的激酶活性, 并磷酸化下游转录因子, 使ABA 信号向下传递, 抑制种子萌发。	Merlot et al., 2001; Raghavendra et al., 2010
		RDO5	RDO5是种子特异性表达的休眠积极调控因子, 独立于ABA对种子休眠的调控, 通过抑制APUM9和APUM11的转录水平调节种子休眠。	Xiang et al., 2014
		FsPP2C1	过表达PP2C1种子萌发率高, 对ABA敏感性低, 且能够在不利的条件 (如甘露醇和盐)下萌发, 通过负调控ABA信号转导, 促进种子萌发。	González-García et al., 2003; Saavedra et al., 2010
		HON	HON通过上调GA合成和响应基因的表达, 下调ABA响应基因和GA分解基因表达, 激活GA信号, 抑制ABA信号, 使种子解除休眠, 向萌发过渡。	Kim et al., 2013
	脂质磷酸酶	LPP2	后熟可激活LPP2的转录活性, 使其表达上调, 抑制种子对ABA的敏感性, 使种子能够完成萌发。	Carrera et al., 2008; Barrero et al., 2009
	线粒体蛋白磷酸酶	SLP2	SLP2与AtMIA40互作, 形成AtSLP2-AtMIA40蛋白质复合体, 通过抑制GA相关过程负调控种子萌发。	Uhrig et al., 2017
	肌醇多聚磷酸1-磷酸酶	FRY1	FRY1突变使IP3大量积累, 导致ABA的诱导和内源RD29A及其它胁迫响应基因的表达显著增强, 负调控ABA和逆境信号, 促进种子萌发。	Xiong et al., 2001

酶	大类	关键基因	分子功能	参考文献
蛋白激酶	MAPKs	MPK8	通过与GA反应的转录因子TCP14相互作用磷酸化TCP14, 增强其转录活性, 调控从休眠到萌发的转换。	Zhang et al., 2019
		MKK1、 MPK6	参与ABA和糖调节的种子萌发, 通过增强ABA的合成与信号强度, 维持种子休眠, 抑制种子萌发。	Xing et al., 2009
		Raf10、 Raf11	过表达Raf10和Raf11, 使种子对ABA敏感性增强, ABI3和ABI5表达上调, 从而延缓种子萌发。	Lee et al., 2015
		MKK3	MKK3-A高表达促进小麦种子休眠释放, 且MKK3可以与Qsd2-AK相互作用, 调控大麦种子休眠。	Nakamura et al., 2016; Torada et al., 2016
	CPKs	CPK4、 CPK11	过表达CPK4和CPK11, 种子表现出对ABA敏感表型, 萌发受到明显抑制。	Zhu et al., 2007
		CPK12	CPK12通过与ABI2相互作用磷酸化ABI2, 并下调ABF1和ABF4表达, 负调控ABA信号, 促进种子萌发。	Zhao et al., 2011a, 2011b
		CPK32	CPK32通过与ABF4相互作用磷酸化ABF4, 增强其转录活性, 促进ABA信号转导, 抑制种子萌发。	Choi et al., 2005
	SnRKs	SnRK2.2、 SnRK2.3	ABA信号通路复合物PYLs-ABA-PP2C通过激活SnRK2.2和SnRK2.3激酶活性, 激活下游转录因子, 诱导种子对ABA的响应。	Finkelstein et al., 2008; Fujii and Zhu, 2009
		SAPK2	ABA受体PYL/RCAR5作用于SAPK2上游, 激活SAPK2激酶活性, 通过OREB1介导ABA信号转导, 激活ABRE启动子活性, 负调控种子萌发。	Kim et al., 2012
类受体激酶	RLKs	GRACE	编码膜蛋白, 在干种子中高表达, 其表达水平受ABA诱导, 进而延缓种子萌发, 维持种子休眠。	Wu et al., 2017
		RPK1	RPK1基因表达受ABA诱导, 通过正调控ABA信号传导, 抑制种子萌发。	Hong et al., 1997; Osakabe et al., 2005
		CRK28	CRK28能够上调ABI3和ABI5的表达, 使ABA反应增强, 削弱种子萌发。	Pelagio-Flores et al., 2019
		CRK45	过表达CRK45能够上调ABA合成及反应基因表达水平, 正调控ABA信号转导, 延缓种子萌发。	Zhang et al., 2013
		CARK1、 CARK6	CARK1和CARK6通过与ABA受体RCAR11-14相互作用, 使其磷酸化, 促进ABA信号转导, 最终抑制种子萌发。	Zhang et al., 2018; Wang et al., 2019
		OsLecRK	OsLecRK表达受萌发信号刺激而上调, 进而与OsADF相互作用, 并进一步转导萌发信号, 上调α-淀粉酶基因表达, 增强种子活力, 促进种子萌发。	Cheng et al., 2013
磷酸酶	PP2Cs	AHG1、 AHG3	DOG1与AHG1/AHG3相互作用, 形成PP2C磷酸酶复合物, 抑制其磷酸酶活性, 进而增强ABA信号, 促使种子休眠。	Née et al., 2017; Nishimura et al., 2018
		PP2C-a10	PP2C-a10与TaDOG1L1和TaDOG1L4互作, 促进小麦种子萌发; 也可与ABA反应基因(ABI3、ABI4、ABI5、EM1和EM6)互作, 降低其表达水平, 促进拟南芥种子萌发。	Yu et al., 2020
		ABI1、 ABI2	在ABA存在条件下, ABA与PYR1/PYL/RCAR受体结合, 抑制ABI1和ABI2活性, 激活SnRK2s的激酶活性, 并磷酸化下游转录因子, 使ABA 信号向下传递, 抑制种子萌发。	Merlot et al., 2001; Raghavendra et al., 2010
		RDO5	RDO5是种子特异性表达的休眠积极调控因子, 独立于ABA对种子休眠的调控, 通过抑制APUM9和APUM11的转录水平调节种子休眠。	Xiang et al., 2014
		FsPP2C1	过表达PP2C1种子萌发率高, 对ABA敏感性低, 且能够在不利的条件 (如甘露醇和盐)下萌发, 通过负调控ABA信号转导, 促进种子萌发。	González-García et al., 2003; Saavedra et al., 2010
		HON	HON通过上调GA合成和响应基因的表达, 下调ABA响应基因和GA分解基因表达, 激活GA信号, 抑制ABA信号, 使种子解除休眠, 向萌发过渡。	Kim et al., 2013
	脂质磷酸酶	LPP2	后熟可激活LPP2的转录活性, 使其表达上调, 抑制种子对ABA的敏感性, 使种子能够完成萌发。	Carrera et al., 2008; Barrero et al., 2009
	线粒体蛋白磷酸酶	SLP2	SLP2与AtMIA40互作, 形成AtSLP2-AtMIA40蛋白质复合体, 通过抑制GA相关过程负调控种子萌发。	Uhrig et al., 2017
	肌醇多聚磷酸1-磷酸酶	FRY1	FRY1突变使IP3大量积累, 导致ABA的诱导和内源RD29A及其它胁迫响应基因的表达显著增强, 负调控ABA和逆境信号, 促进种子萌发。	Xiong et al., 2001