The interaction between phytohormones is an important mechanism which controls growth and developmental processes in plants. Deciphering these interactions is a crucial step in helping to develop crops with enhanced yield and resistance to environmental stresses. Controlling the expression level of OsAP2-39 which includes an APETALA 2 (AP2) domain leads to phenotypic changes in rice. Overexpression of OsAP2-39 leads to a reduction in yield by decreasing the biomass and the number of seeds in the transgenic rice lines. Global transcriptome analysis of the OsAP2-39 overexpression transgenic rice revealed the upregulation of a key Abscisic Acid (ABA) biosynthetic gene OsNCED-I which codes for 9-cis-epoxycarotenoid dioxygenase and leads to an increase in the endogenous ABA level. In addition to OsNCED-1, the gene expression analysis revealed the upregulation of a gene that codes for the Elongation of Upper most Internode (EUI) protein, an enzyme that catalyzes 16α, 17-epoxidation of non-13-hydroxylated GAs, which has been shown to deactivate gibberellins (GAs) in rice. The exogenous application of GA restores the wild-type phenotype in the transgenic line and ABA application induces the expression of EUI and suppresses the expression of OsAP2-39 in the wild-type line. These observations clarify the antagonistic relationship between ABA and GA and illustrate a mechanism that leads to homeostasis of these hormones. In vivo and in vitro analysis showed that the expression of both OsNCED-1 and EUI are directly controlled by OsAP2-39. Together, these results reveal a novel mechanism for the control of the ABA/GA balance in rice which is regulated by OsAP2-39 that in turn regulates plant growth and seed production.
References
[1]
Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, et al. (2006) Regulation of hormone metabolism in arabidopsis seeds: Phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48(3): 354–366.
[2]
Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, et al. (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in arabidopsis seeds. Plant Cell 19(4): 1192–1208.
[3]
Cheng WH, Endo A, Zhou L, Penney J, Chen HC, et al. (2002) A unique short-chain dehydrogenase/reductase in arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14(11): 2723–2743.
[4]
Lin PC, Hwang SG, Endo A, Okamoto M, Koshiba T, et al. (2007) Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol 143(2): 745–758.
[5]
Sharp RE (2002) Interaction with ethylene: Changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25(2): 211–222.
Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, et al. (2007) Global analysis of della direct targets in early gibberellin signaling in arabidopsis. Plant Cell 19(10): 3037–3057.
[8]
Johnson RR, Shin M, Shen JQ (2008) The wheat PKABA1-interacting factor TaABF1 mediates both abscisic acid-suppressed and abscisic acid-induced gene expression in bombarded aleurone cells. Plant Mol Biol 68(1–2): 93–103.
[9]
Shen Q, Gomez-Cadenas A, Zhang P, Walker-Simmons MK, Sheen J, et al. (2001) Dissection of abscisic acid signal transduction pathways in barley aleurone layers. Plant Mol Biol 47(3): 437–448.
[10]
Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) The transcription factor FUSCA3 controls developmental timing in arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7(3): 373–385.
[11]
Curaba J, Moritz T, Blervaque R, Parcy F, Raz V, et al. (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in arabidopsis. Plant Physiol 136(3): 3660–3669.
[12]
Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: Biosynthesis, catabolism, and response pathways. Plant Cell 14: SupplS61–80.
[13]
Razem FA, Baron K, Hill RD (2006) Turning on gibberellin and abscisic acid signaling. Curr Opin Plant Biol 9(5): 454–459.
[14]
Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55: 197–223.
[15]
Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379(6): 633–646.
[16]
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in arabidopsis and rice. Plant Physiol 140(2): 411–432.
[17]
Shukla RK, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol 142(1): 113–123.
[18]
Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic virginia pine (pinus virginiana mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59(4): 603–617.
[19]
Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2004) Dwarf and delayed-flowering 1, a novel arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J 37(5): 720–729.
[20]
Ward JM, Smith AM, Shah PK, Galanti SE, Yi H, et al. (2006) A new role for the arabidopsis AP2 transcription factor, LEAFY PETIOLE, in gibberellin-induced germination is revealed by the misexpression of a homologous gene, SOB2/DRN-LIKE. Plant Cell 18(1): 29–39.
[21]
Wu L, Chen X, Ren H, Zhang Z, Zhang H, et al. (2007) ERF protein JERF1 that transcriptionally modulates the expression of abscisic acid biosynthesis-related gene enhances the tolerance under salinity and cold in tobacco. Planta 226(4): 815–825.
[22]
Zhang Y, Zhu Y, Peng Y, Yan D, Li Q, et al. (2008) Gibberellin homeostasis and plant height control by EUI and a role for gibberellin in root gravity responses in rice. Cell Res 18(3): 412–421.
[23]
Ma H, Zhang S, Ji L, Zhu H, Yang S, et al. (2006) Fine mapping and in silico isolation of the EUI1 gene controlling upper internode elongation in rice. Plant Mol Biol 60(1): 87–94.
[24]
Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, et al. (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18(2): 442–456.
[25]
Degenhardt J, Poppe A, Montag J, Szankowski I (2006) The use of the phosphomannose-isomerase/mannose selection system to recover transgenic apple plants. Plant Cell Rep 25(11): 1149–1156.
[26]
Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, et al. (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134(4): 1642–1653.
[27]
Ashikari M, Wu J, Yano M, Sasaki T, Yoshimura A (1999) Rice gibberellin-insensitive dwarf mutant gene dwarf 1 encodes the alpha-subunit of GTP-binding protein. Proc Natl Acad Sci U S A 96(18): 10284–10289.
[28]
Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, et al. (2002) Green revolution: A mutant gibberellin-synthesis gene in rice. Nature 416(6882): 701–702.
[29]
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, et al. (2001) Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13(5): 999–1010.
[30]
Komorisono M, Ueguchi-Tanaka M, Aichi I, Hasegawa Y, Ashikari M, et al. (2005) Analysis of the rice mutant dwarf and gladius leaf 1. aberrant katanin-mediated microtubule organization causes up-regulation of gibberellin biosynthetic genes independently of gibberellin signaling. Plant Physiol 138(4): 1982–1993.
[31]
Iuchi S, Suzuki H, Kim YC, Iuchi A, Kuromori T, et al. (2007) Multiple loss-of-function of arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50(6): 958–966.
[32]
McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, et al. (2003) The arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15(5): 1120–1130.
[33]
Dill A, Thomas SG, Hu J, Steber CM, Sun TP (2004) The arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16(6): 1392–1405.
[34]
Sun T, Goodman HM, Ausubel FM (1992) Cloning the arabidopsis GA1 locus by genomic subtraction. Plant Cell 4(2): 119–128.
[35]
Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276(5320): 1872–1874.
[36]
Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7(1): 41–48.
[37]
Qin X, Zeevaart JA (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci U S A 96(26): 15354–15361.
[38]
Jung KH, Lee J, Dardick C, Seo YS, Cao P, et al. (2008) Identification and functional analysis of light-responsive unique genes and gene family members in rice. PLoS Genet 4(8): e1000164.
[39]
Audran C, Borel C, Frey A, Sotta B, Meyer C, et al. (1998) Expression studies of the zeaxanthin epoxidase gene in nicotiana plumbaginifolia. Plant Physiol 118(3): 1021–1028.
[40]
Schomburg FM, Bizzell CM, Lee DJ, Zeevaart JA, Amasino RM (2003) Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell 15(1): 151–163.
[41]
Wang H, Caruso LV, Downie AB, Perry SE (2004) The embryo MADS domain protein AGAMOUS-like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 16(5): 1206–1219.
[42]
Oliver SN, Dennis ES, Dolferus R (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol 48(9): 1319–1330.
[43]
Zimmermann P, Hennig L, Gruissem W (2005) Gene-expression analysis and network discovery using genevestigator. Trends Plant Sci 10(9): 407–409.
[44]
Kiseleva IS, Kaminskaya OA (2002) Hormonal regulation of assimilate utilization in barley leaves in relation to the development of their source function. RUSSIAN JOURNAL OF PLANT PHYSIOLOGY 49(4): 534–540.
[45]
Yu H, Chen X, Hong Y, Wang Y, Xu P, et al. (2008) Activated expression of an arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell.
[46]
Thompson AJ, Andrews J, Mulholland BJ, McKee JM, Hilton HW, et al. (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiol 143(4): 1905–1917.
[47]
Voisin AS, Reidy B, Parent B, Rolland G, Redondo E, et al. (2006) Are ABA, ethylene or their interaction involved in the response of leaf growth to soil water deficit? an analysis using naturally occurring variation or genetic transformation of ABA production in maize. Plant Cell Environ 29(9): 1829–1840.
[48]
Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, et al. (2006) The arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16(6): 553–563.
[49]
Lazar G, Goodman HM (2006) MAX1, a regulator of the flavonoid pathway, controls vegetative axillary bud outgrowth in arabidopsis. Proc Natl Acad Sci U S A 103(2): 472–476.
[50]
Booker J, Sieberer T, Wright W, Williamson L, Willett B, et al. (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8(3): 443–449.
[51]
Stirnberg P, van De Sande K, Leyser HM (2002) MAX1 and MAX2 control shoot lateral branching in arabidopsis. Development 129(5): 1131–1141.
[52]
Li X, Qian Q, Fu Z, Wang Y, Xiong G, et al. (2003) Control of tillering in rice. Nature 422(6932): 618–621.
[53]
Oliver SN, Zhao X, Dennis ES, Dolferus R (2008) The molecular basis of cold-induced pollen sterility in rice. Biotechnology and Sustainable Agriculture 2006 and Beyond 205–207.
[54]
Bi YM, Zhang Y, Signorelli T, Zhao R, Zhu T, et al. (2005) Genetic analysis of arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. Plant J 44(4): 680–692.
[55]
Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45(4): 490–495.
[56]
Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138(4): 1903–1913.
[57]
Chiwocha SD, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, et al. (2005) The etr1-2 mutation in arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42(1): 35–48.
[58]
Rieu I, Ruiz-Rivero O, Fernandez-Garcia N, Griffiths J, Powers SJ, et al. (2008) The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the arabidopsis life cycle. Plant J 53(3): 488–504.
[59]
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8): 1596–1599.
[60]
Jefferson R (1987) Assaying chimeric genes in plants: The GUS gene fusion system. Plant Molecular Biology Reporter 5(4): 387–405.
