Abstract
Plant architecture directly affects biomass in higher plants, especially grain yields in agricultural crops. In this study, we characterized a recessive mutant, plant architecture determinant (pad), derived from the Oryza sativa ssp. indica cultivar MH86. The mutant exhibited severe dwarf phenotypes, including shorter and stunted leaves, fewer secondary branches during both the vegetative and reproductive growth stages. Cytological studies revealed that pad mutant growth defects are primarily due to the inhibition of cell expansion. The PAD gene was isolated using a map-based cloning strategy. It encodes a plasma membrane protein OsMCA1 and a SNP responsible for a single amino acid change was found in the mutant. PAD was universally expressed in rice tissues from the vegetative to reproductive growth stages, especially in seedlings, nodes and rachillae. Quantitative real-time PCR analysis revealed that the most of the genes responding to gibberellin (GA) metabolism were up-regulated in pad mutant internodes. The endogenous GA content measurement revealed that the levels of GA1 were significantly decreased in the third internode of pad mutants. Moreover, a GA response assay suggested that OsMCA1/PAD might be involved in the regulation of GA metabolism and signal transduction. Our results revealed the pad is a loss-of-function mutant of the OsMCA1/PAD, leading to upregulation of genes related to GA deactivation, which decreased bioactive GA levels.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ashikari M, Sasaki A, Ueguchi-Tanaka M, Itoh H, Nishimura A, Datta S, Ishiyama K, Saito T, Kobayashi M, Khush GS (2002) Loss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), led to the rice ‘green revolution’. Breed Sci 52:143–150
Chen ML, Fu XM, Liu JQ, Ye TT, Hou SY, Huang YQ, Yuan BF, Wu Y, Feng YQ (2012) Highly sensitive and quantitative profiling of acidic phytohormones using derivatization approach coupled with nano-LC-ESI-Q-TOF-MS analysis. J Chromatogr B Analyt Technol Biomed Life Sci 905:67–74
Cong B, Liu J, Tanksley SD (2002) Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. Proc Natl Acad Sci USA 99:13606–13611
Dai M, Zhao Y, Ma Q, Hu Y, Hedden P, Zhang Q, Zhou DX (2007) The rice YABBY1 gene is involved in the feedback regulation of gibberellin metabolism. Plant Physiol 144:121–133
Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
Guo M, Rupe MA, Dieter JA, Zou J, Spielbauer D, Duncan KE, Howard RJ, Hou Z, Simmons CR (2010) Cell Number Regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell 22:1057–1073
Guo X, Hou X, Fang J, Wei P, Xu B, Chen M, Feng Y, Chu C (2013) The rice GERMINATION DEFECTIVE 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism. Plant J 75:403–416
Hattan J, Kanamoto H, Takemura M, Yokota A, Kohchi T (2004) Molecular characterization of the cytoplasmic interacting protein of the receptor kinase IRK expressed in the inflorescence and root apices of Arabidopsis. Biosci Biotechnol Biochem 68:2598–2606
Hedden P, Thomas SG (2012) Gibberellin biosynthesis and its regulation. Biochem J 444:11–25
Huang J, Tang D, Shen Y, Qin B, Hong L, You A, Li M, Wang X, Yu H, Gu M, Cheng Z (2010) Activation of gibberellin 2-oxidase 6 decreases active gibberellin levels and creates a dominant semi-dwarf phenotype in rice (Oryza sativa L.). J Genet Genomics 37:23–36
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (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 13:999–1010
Itoh H, Tatsumi T, Sakamoto T, Otomo K, Toyomasu T, Kitano H, Ashikari M, Ichihara S, Matsuoka M (2004) A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase. Plant Mol Biol 54:533–547
Jefferson RA (1989) The GUS reporter gene system. Nature 342:837–838
Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544
Jin J, Huang W, Gao JP, Yang J, Shi M, Zhu MZ, Luo D, Lin HX (2008) Genetic control of rice plant architecture under domestication. Nat Genet 40:1365–1369
Kesavapany S, Lau KF, Ackerley S, Banner SJ, Shemilt SJ, Cooper JD, Leigh PN, Shaw CE, McLoughlin DM, Miller CC (2003) Identification of a novel, membrane-associated neuronal kinase, cyclin-dependent kinase 5/p35-regulated kinase. J Neurosci 23:4975–4983
Kurusu T, Nishikawa D, Yamazaki Y, Gotoh M, Nakano M, Hamada H, Yamanaka T, Iida K, Nakagawa Y, Saji H, Shinozaki K, Iida H, Kuchitsu K (2012) Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca2 + influx and modulates generation of reactive oxygen species in cultured rice cells. BMC Plant Biol 12:11
Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621
Li P, Wang Y, Qian Q, Fu Z, Wang M, Zeng D, Li B, Wang X, Li J (2007) LAZY1 controls rice shoot gravitropism through regulating polar auxin transport. Cell Res 17:402–410
Magome H, Nomura T, Hanada A, Takeda-Kamiya N, Ohnishi T, Shinma Y, Katsumata T, Kawaide H, Kamiya Y, Yamaguchi S (2013) CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proc Natl Acad Sci USA 110:1947–1952
Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549
Nakagawa Y, Katagiri T, Shinozaki K, Qi Z, Tatsumi H, Furuichi T, Kishigami A, Sokabe M, Kojima I, Sato S, Kato T, Tabata S, Iida K, Terashima A, Nakano M, Ikeda M, Yamanaka T, Iida H (2007) Arabidopsis plasma membrane protein crucial for Ca2 + influx and touch sensing in roots. Proc Natl Acad Sci USA 104:3639–3644
Nakano M, Iida K, Nyunoya H, Iida H (2011) Determination of structural regions important for Ca(2+) uptake activity in Arabidopsis MCA1 and MCA2 expressed in yeast. Plant Cell Physiol 52:1915–1930
Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14(Suppl):S61–S80
Sakamoto T (2006) Phytohormones and rice crop yield: strategies and opportunities for genetic improvement. Transgenic Res 15:399–404
Sakamoto T, Matsuoka M (2004) Generating high-yielding varieties by genetic manipulation of plant architecture. Curr Opin Biotechnol 15:144–147
Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K, Miyao A, Hirochika H, Kitano H, Ashikari M, Matsuoka M (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134:1642–1653
Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat Biotechnol 24:105–109
Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS, Kitano H, Matsuoka M (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416:701–702
Springer N (2010) Shaping a better rice plant. Nat Genet 42:475–476
Takeda K (1979) Internode elongation and dwarfism in some gramineous plants. Gamma field symp 16:1–18
Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33:513–520
Tan L, Li X, Liu F, Sun X, Li C, Zhu Z, Fu Y, Cai H, Wang X, Xie D, Sun C (2008) Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet 40:1360–1364
Thomas SG, Rieu I, Steber CM (2005) Gibberellin metabolism and signaling. Vitam Horm 72:289–338
Tsuwamoto R, Fukuoka H, Takahata Y (2008) GASSHO1 and GASSHO2 encoding a putative leucine-rich repeat transmembrane-type receptor kinase are essential for the normal development of the epidermal surface in Arabidopsis embryos. Plant J 54:30–42
Uchida N, Igari K, Bogenschutz NL, Torii KU, Tasaka M (2011) Arabidopsis ERECTA-family receptor kinases mediate morphological alterations stimulated by activation of NB-LRR-type UNI proteins. Plant Cell Physiol 52:804–814
Ueguchi-Tanaka M, Fujisawa Y, Kobayashi M, Ashikari M, Iwasaki Y, Kitano H, Matsuoka M (2000) Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA 97:11638–11643
Wang Y, Li J (2005) The plant architecture of rice (Oryza sativa). Plant Mol Biol 59:75–84
Wang Y, Li J (2008) Rice, rising. Nat Genet 40:1273–1275
Wiens M, Korzhev M, Perovic-Ottstadt S, Luthringer B, Brandt D, Klein S, Muller WE (2007) Toll-like receptors are part of the innate immune defense system of sponges (demospongiae: porifera). Mol Biol Evol 24:792–804
Wu X, Tang D, Li M, Wang K, Cheng Z (2013) Loose Plant Architecture1, an INDETERMINATE DOMAIN protein involved in shoot gravitropism, regulates plant architecture in rice. Plant Physiol 161:317–329
Xing Y, Zhang Q (2010) Genetic and molecular bases of rice yield. Annu Rev Plant Biol 61:421–442
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
Yamanaka T, Nakagawa Y, Mori K, Nakano M, Imamura T, Kataoka H, Terashima A, Iida K, Kojima I, Katagiri T, Shinozaki K, Iida H (2010) MCA1 and MCA2 that mediate Ca2 + uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol 152:1284–1296
Yang XC, Hwa CM (2008) Genetic modification of plant architecture and variety improvement in rice. Heredity 101:396–404
Yoshihara T, Iino M (2007) Identification of the gravitropism-related rice gene LAZY1 and elucidation of LAZY1-dependent and -independent gravity signaling pathways. Plant Cell Physiol 48:678–688
Yu B, Lin Z, Li H, Li X, Li J, Wang Y, Zhang X, Zhu Z, Zhai W, Wang X, Xie D, Sun C (2007) TAC1, a major quantitative trait locus controlling tiller angle in rice. Plant J 52:891–898
Zhang Q, Li J, Xue Y, Han B, Deng XW (2008) Rice 2020: a call for an international coordinated effort in rice functional genomics. Mol Plant 1:715–719
Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442–456
Acknowledgments
We thank Prof. Yu-Qi Feng for technical assistance of GA content analysis. This work was supported by the National Natural Science Foundation of China (No.3087496).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, Z., Cheng, Q., Sun, Y. et al. A SNP in OsMCA1 responding for a plant architecture defect by deactivation of bioactive GA in rice. Plant Mol Biol 87, 17–30 (2015). https://doi.org/10.1007/s11103-014-0257-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-014-0257-y