植物内源ABA水平的动态调控机制

doi:10.11983/CBB19092

摘要/Abstract

摘要： ABA具有调节植物生长发育和对环境胁迫做出快速反应的重要功能, 植物内源ABA水平受到ABA合成、代谢及转运等途径的复杂调控。该文综述了近年来植物ABA从头合成、羟基化代谢、可逆糖基化代谢及ABA转运等领域的最新研究进展, 重点讨论ABA合成与代谢基因的表达调控机制, 并展望了今后的研究方向。

关键词: 脱落酸, ABA合成, ABA代谢, ABA转运

Abstract: Abscisic acid (ABA) plays important roles in regulating plant growth and development, and in responding rapidly to various environmental stimuli. The endogenous ABA level in plants is regulated sophisticatedly by the ABA biosynthesis, catabolism, and transportation pathways. This paper reviewed the most recent advancements in ABA de novo biosynthesis, ABA hydroxylation catabolism, reversible glycosylation metabolism, and ABA transportation pathway in plants, with emphasis on the expression regulation mechanism of the ABA biosynthetic and catabolic genes. Prospectives for research directions in the future were also suggested.

Key words: abscisic acid, ABA biosynthesis, ABA metabolism, ABA transportation

陈唯,曾晓贤,谢楚萍,田长恩,周玉萍. 植物内源ABA水平的动态调控机制. 植物学报, 2019, 54(6): 677-687.

Wei Chen,Xiaoxian Zeng,Chuping Xie,Chang’en Tian,Yuping Zhou. The Dynamic Regulation Mechanism of the Endo-genous ABA in Plant. Chinese Bulletin of Botany, 2019, 54(6): 677-687.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB19092

https://www.chinbullbotany.com/CN/Y2019/V54/I6/677

图/表 1

参考文献 79

[1]	任慧波, 范意娟, 魏开发, 高志晖, 李桂芬, 刘静, 李冰冰, 胡建芳, 贾文锁 (2007). NCED3基因的持续诱导及ABA合成与代谢的协同调控在拟南芥ABA信号积累中的作用. 科学通报 52, 59-66.
[2]	魏开发, 陈娟, 陈艳峰, 吴凌娟, 贾文锁 ( 2012). 内源ABA信号水平动态调控的分子机制. 遗传 34, 296-306.
[3]	伍静辉, 谢楚萍, 田长恩, 周玉萍 ( 2018). 脱落酸调控种子休眠和萌发的分子机制. 植物学报 53, 542-555.
[4]	Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, Ponce MR, Micol JL ( 2005). A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56, 2071-2083.
[5]	Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-Rasheid KA, Sonnewald S, Sonnewald U, Kneitz S, Lachmann N, Mendel RR, Bittner F, Hetherington AM, Hedrich R ( 2013). The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr Biol 23, 53-57.
[6]	Boursiac Y, Leran S, Corratgé-Faillie C, Gojon A, Krouk G, Lacombe B ( 2013). ABA transport and transporters. Trends Plant Sci 18, 325-333.
[7]	Cao MJ, Wang Z, Zhao Q, Mao JL, Speiser A, Wirtz M, Hell R, Zhu JK, Xiang CB ( 2014). Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77, 604-615.
[8]	Chen HY, Hsieh EJ, Cheng MC, Chen CY, Hwang SY, Lin TP ( 2016). ORA47 (octadecanoid-responsive AP2/ERF- domain transcription factor 47) regulates jasmonic acid and abscisic acid biosynthesis and signaling through binding to a novel cis-element. New Phytol 211, 599-613.
[9]	Cui P, Zhang S, Ding F, Ali S, Xiong L ( 2014). Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis. Genome Biol 15, R1.
[10]	Dong T, Xu ZY, Park Y, Kim DH, Lee Y, Hwang I ( 2014). Abscisic acid uridine diphosphate glucosyltransferases play a crucial role in abscisic acid homeostasis in Arabidopsis. Plant Physiol 165, 277-289.
[11]	Endo A, Okamoto M, Koshiba T (2014). ABA biosynthetic and catabolic pathways. In: Zhang DP, ed. Abscisic Acid: Metabolism, Transport and Signaling. Dordrecht: Springer Press. pp. 21-45.
[12]	Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E ( 2008). Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147, 1984-1993.
[13]	Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A ( 2012). Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70, 501-512.
[14]	Hao GP, Zhang XH, Wang YQ, Wu ZY, Huang CL ( 2009). Nucleotide variation in the NCED3 region of Arabidopsis thaliana and its association study with abscisic acid content under drought stress. J Integr Plant Biol 51, 175-183.
[15]	Harrison E, Burbidge A, Okyere JP, Thompson AJ, Taylor IB ( 2011). Identification of the tomato ABA-deficient mutant sitiens as a member of the ABA-aldehyde oxidase gene family using genetic and genomic analysis. Plant Growth Regul 64, 301-309.
[16]	Je J, Chen H, Song C, Lim CO ( 2014). Arabidopsis DREB2C modulates ABA biosynthesis during germination. Biochem Biophys Res Commun 452, 91-98.
[17]	Jensen MK, Lindemose S, de Masi F, Reimer JJ, Nielsen M, Perera V, Workman CT, Turck F, Grant MR, Mundy J, Petersen M, Skriver K ( 2013). ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Biol 3, 321-327.
[18]	Jiang YJ, Liang G, Yu DQ ( 2012). Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol Plant 5, 1375-1388.
[19]	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, 2355-2360.
[20]	Kang J, Yim S, Choi H, Kim A, Lee KP, Lopez-Molina L, Martinoia E, Lee Y ( 2015). Abscisic acid transporters cooperate to control seed germination. Nat Commun 6, 8113.
[21]	Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M ( 2012). Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci USA 109, 9653-9658.
[22]	Ko JH, Yang SH, Han KH ( 2006). Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47, 343-355.
[23]	Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T ( 2004). Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiol 134, 1697-1707.
[24]	Kuromori T, Fujita M, Urano K, Tanabata T, Sugimoto E, Shinozaki K ( 2016). Overexpression of AtABCG25 enhances the abscisic acid signal in guard cells and improves plant water use efficiency. Plant Sci 251, 75-81.
[25]	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, 2361-2366.
[26]	Kuromori T, Seo M, Shinozaki K ( 2018). ABA transport and plant water stress responses. Trends Plant Sci 23, 513-522.
[27]	Kuromori T, Sugimoto E, Shinozaki K ( 2011). Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67, 885-894.
[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, 1647-1656.
[29]	Le Hir R, Castelain M, Chakraborti D, Moritz T, Dinant S, Bellini C ( 2017). At bHLH68 transcription factor contributes to the regulation of ABA homeostasis and drought stress tolerance in Arabidopsis thaliana. Physiol Plant 160, 312-327.
[30]	Lee HG, Lee K, Seo PJ ( 2015). The Arabidopsis MYB96 transcription factor plays a role in seed dormancy. Plant Mol Biol 87, 371-381.
[31]	Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I ( 2006). Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126, 1109-1120.
[32]	Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A ( 2006). Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45, 309-319.
[33]	Li W, De Ollas C, Dodd IC ( 2018). Long-distance ABA transport can mediate distal tissue responses by affecting local ABA concentrations. J Integr Plant Biol 60, 16-33.
[34]	Lin PC, Hwang SG, Endo A, Okamoto M, Koshiba T, Cheng WH ( 2007). Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol 143, 745-758.
[35]	Lisso J, Schröder F, Fisahn J, Müssig C ( 2011). NFX1-LIKE2 (NFXL2) suppresses abscisic acid accumulation and stomatal closure in Arabidopsis thaliana. PLoS One 6, e26982.
[36]	Lisso J, Schröder F, Schippers JHM, Müssig C ( 2012). Nfxl2 modifies cuticle properties in Arabidopsis. Plant Signaling Behavior 7, 551-555.
[37]	Liu S, Li M, Su L, Ge K, Li L, Li X, Liu X, Li L ( 2016). Negative feedback regulation of ABA biosynthesis in peanut (Arachis hypogaea): a transcription factor complex inhibits AhNCED1 expression during water stress. Sci Rep 6, 37943.
[38]	Liu W, Tai H, Li S, Gao W, Zhao M, Xie C, Li WX ( 2014). bHLH122 is important for drought and osmotic stress resistance in Arabidopsis and in the repression of ABA catabolism. New Phytol 201, 1192-1204.
[39]	Liu Z, Yan JP, Li DK, Luo Q, Yan Q, Liu ZB, Ye LM, Wang JM, Li XF, Yang Y ( 2015). UDP-glucosyltransferase71C5, a major glucosyltransferase, mediates abscisic acid homeostasis in Arabidopsis. Plant Physiol 167, 1659-1670.
[40]	Ma YL, Cao J, He JH, Chen QQ, Li XF, Yang Y ( 2018). Molecular mechanism for the regulation of ABA homeostasis during plant development and stress responses. Int J Mol Sci 19, 3643.
[41]	Malcheska F, Ahmad A, Batool S, Müller HM, Ludwig- Müller J, Kreuzwieser J, Randewig D, Hänsch R, Mendel RR, Hell R, Wirtz M, Geiger D, Ache P, Hedrich R, Herschbach C, Rennenberg H ( 2017). Drought-enhanced xylem sap sulfate closes stomata by affecting ALMT12 and guard cell ABA synthesis. Plant Physiol 174, 798-814.
[42]	Matakiadis T, Alboresi A, Jikumaru Y, Tatematsu K, Pichon O, Renou JP, Kamiya Y, Nambara E, Truong HN ( 2009). The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiol 149, 949-960.
[43]	Nambara E, Marion-Poll A ( 2005). Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56, 165-185.
[44]	North HM, De Almeida A, Boutin JP, Frey A, To A, Botran L, Sotta B, Marion-Poll A ( 2007). The Arabidopsis ABA- deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. Plant J 50, 810-824.
[45]	Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E ( 2006). CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141, 97-107.
[46]	Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E ( 2009). High humidity induces abscisic acid 8′-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiol 149, 825-834.
[47]	Park HY, Seok HY, Park BK, Kim SH, Goh CH, Lee BH, Lee CH, Moon YH ( 2008). Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress. Biochem Biophys Res Commun 375, 80-85.
[48]	Park Y, Xu ZY, Kim SY, Lee J, Choi B, Lee J, Kim H, Sim HJ, Hwang I ( 2016). Spatial regulation of ABCG25, an ABA exporter, is an important component of the mechanism controlling cellular ABA levels. Plant Cell 28, 2528-2544.
[49]	Perea-Resa C, Carrasco-López C, Catalá R, Turečková V, Novak O, Zhang W, Sieburth L, Jiménez-Gómez JM, Salinas J ( 2016). The LSM1-7 complex differentially regulates Arabidopsis tolerance to abiotic stress conditions by promoting selective mRNA decapping. Plant Cell 28, 505-520.
[50]	Priest DM, Ambrose SJ, Vaistij FE, Elias L, Higgins GS, Ross ARS, Abrams S, Bowles DJ ( 2006). Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J 46, 492-502.
[51]	Ren T, Wang J, Zhao M, Gong X, Wang S, Wang G, Zhou C ( 2018). Involvement of NAC transcription factor SiNAC1 in a positive feedback loop via ABA biosynthesis and leaf senescence in foxtail millet. Planta 247, 53-68.
[52]	Sato H, Takasaki H, Takahashi F, Suzuki T, Iuchi S, Mitsuda N, Ohme-Takagi M, Ikeda M, Seo M, Yamaguchi-Shinozaki K, Shinozaki K ( 2018). Arabidopsis thaliana NGATHA1 transcription factor induces ABA biosynthesis by activating NCED3 gene during dehydration stress. Proc Natl Acad Sci USA 115, E11178-E11187.
[53]	Scholz SS, Reichelt M, Vadassery J, Mithöfer A ( 2015). Calmodulin-like protein CML37 is a positive regulator of ABA during drought stress in Arabidopsis. Plant Signal Behav 10, e1011951.
[54]	Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR ( 1997). Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276, 1872-1874.
[55]	Seo M, Aoki K, 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, 1694-1703.
[56]	Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Liu C, Feng Y, Cao X, Xie Q ( 2013). ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet 9, e1003577.
[57]	Sussmilch FC, Brodribb TJ, Mcadam SAM ( 2017). Up-regulation of NCED3 and ABA biosynthesis occur within minutes of a decrease in leaf turgor but AHK1 is not required. J Exp Bot 68, 2913-2918.
[58]	Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K ( 2018). A small peptide modulates stomatal control via abscisic acid in long-distance signaling. Nature 556, 235-238.
[59]	Tan BC, Joseph LM, Deng WT, Liu LJ, Li QB, Cline K, McCarty DR ( 2003). Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35, 44-56.
[60]	Tan BC, Schwartz SH, Zeevaart JAD, Mccarty DR ( 1997). Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94, 12235-12240.
[61]	Tan WR, Zhang DW, Zhou HP, Zheng T, Yin YH, Lin HH ( 2018). Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought. PLoS Genet 14, e1007336.
[62]	Tsugama D, Liu SK, Takano T ( 2012). A bZIP protein, VIP1, is a regulator of osmosensory signaling in Arabidopsis. Plant Physiol 159, 144-155.
[63]	Umezawa T, Okamoto M, Kushiro T, Nambara E, Oono Y, Seki M, Kobayashi M, Koshiba T, Kamiya Y, Shinozaki K ( 2006). CYP707A3, a major ABA 80-hydroxylase involved in dehydration and rehydration response in Arabido- psis thaliana. Plant J 46, 171-182.
[64]	Vallabhaneni R, Wurtzel ET ( 2010). From epoxycarotenoids to ABA: the role of ABA 8′-hydroxylases in drought- stressed maize roots. Arch Biochem Biophys 504, 112-117.
[65]	Wang PT, Liu H, Hua HJ, Wang L, Song CP ( 2011a). A vacuole localized β-glucosidase contributes to drought tolerance in Arabidopsis. Chin Sci Bull 56, 3538-3546.
[66]	Wang Z, Wang FX, Hong YC, Yao JJ, Ren ZZ, Shi HZ, Zhu JK ( 2018). The flowering repressor SVP confers drought resistance in Arabidopsis by regulating abscisic acid catabolism. Mol Plant 11, 1184-1197.
[67]	Wang ZY, Xiong L, Li W, Zhu JK, Zhu J ( 2011b). The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. Plant Cell 23, 1971-1984.
[68]	Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK ( 2001). Modulation of abscisic acid signal transduction and biosynthesis by an smlike protein in Arabidopsis. Cell 1, 771-781.
[69]	Xu ZJ, Nakajima M, Suzuki Y, Yamaguchi I ( 2002). Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings. Plant Physiol 129, 1285-1295.
[70]	Xu ZY, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA, Yun DJ, Hwang I ( 2012). A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24, 2184-2199.
[71]	Yan D, Easwaran V, Chau V, Okamoto M, Ierullo M, Kimura M, Endo A, Yano R, Pasha A, Gong Y, Bi YM, Provart N, Guttman D, Krapp A, Rothstein SJ, Nambara E ( 2016). NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis. Nat Commun 7, 13179.
[72]	Yang J, Worley E, Udvardi M ( 2014). A NAP-AAO3 regulatory module promotes chlorophyll degradation via ABA biosynthesis in Arabidopsis leaves. Plant Cell 26, 4862-4874.
[73]	Yano R, Kanno Y, Jikumaru Y, Nakabayashi K, Kamiya Y, Nambara E ( 2009). CHOTTO1, a putative double APETALA2 repeat transcription factor, is involved in abscisic acid-mediated repression of gibberellin biosynthesis during seed germination in Arabidopsis. Plant Physiol 151, 641-654.
[74]	Yue Y, Zhang M, Zhang J, Tian X, Duan L, Li Z ( 2012). Overexpression of the AtLOS5 gene increased abscisic acid level and drought tolerance in transgenic cotton. J Exp Bot 63, 3741-3748.
[75]	Zdunek-Zastocka E, Sobczak M ( 2013). Expression of Pisum sativum PsAO3 gene, which encodes an aldehyde oxidase utilizing abscisic aldehyde, is induced under progressively but not rapidly imposed drought stress. Plant Physiol Biochem 71(2), 57-66.
[76]	Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L ( 2014). A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol Plant 7, 1522-1532.
[77]	Zhou YP, Wu JH, Xiao WH, Chen W, Chen QH, Fan T, Xie CP, Tian CE ( 2018). Arabidopsis IQM4, a novel calmodulin-binding protein, is involved with seed dormancy and germination in Arabidopsis. Front Plant Sci 9, 721.
[78]	Zhu G, Ye N, Zhang J ( 2009). Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50, 644-651.
[79]	Chen W, Zeng XX, Xie CP, Tian CE, Zhou YP ( 2019). The dynamic regulation mechanism of the endogenous ABA in plant. Chin Bull Bot 54, 677-687.