Abstract
Jasmonates are important phytohormones regulating reproductive development. We used two recessive rice Tos17 alleles of OsJAR1, osjar1-2 and osjar1-3, to study the biological function of jasmonates in rice anthesis. The florets of both osjar1 alleles stayed open during anthesis because the lodicules, which control flower opening in rice, were not withering on time. Furthermore, dehiscence of the anthers filled with viable pollen, was impaired, resulting in lower fertility. In situ hybridization and promoter GUS transgenic analysis confirmed OsJAR1 expression in these floral tissues. Flower opening induced by exogenous applied methyl jasmonate was impaired in osjar1 plants and was restored in a complementation experiment with transgenics expressing a wild type copy of OsJAR1 controlled by a rice actin promoter. Biochemical analysis showed that OsJAR1 encoded an enzyme conjugating jasmonic acid (JA) to at least Ile, Leu, Met, Phe, Trp and Val and both osjar1 alleles had substantial reduction in content of JA-Ile, JA-Leu and JA-Val in florets. We conclude that OsJAR1 is a JA-amino acid synthetase that is required for optimal flower opening and closing and anther dehiscence in rice.
Similar content being viewed by others
Abbreviations
- AA:
-
Amino acid
- GUS:
-
β-glucuronidase
- Ile:
-
Isoleucine
- JA:
-
Jasmonic acid
- JAR1:
-
Jasmonate resistant 1
- JA-Ile:
-
Jasmonoyl-l-isoleucine
- ORF:
-
Open reading frame
- MeJA:
-
Methyl jasmonate
References
Alberts B, Wilson JH, Hunt T (2008) Molecular biology of the cell. Garland Science, New York
Bieleski R, Elgar J, Heyes J (2000) Mechanical aspects of rapid flower opening in Asiatic Lily. Ann Bot 86:1175–1183
Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk PB, An G, Colombo L, Kater MM (2007) The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J 52:690–699
Farmer EE (2007) Plant biology: jasmonate perception machines. Nature 448:659–660
Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano 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. Plant Cell 23:701–715
Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350
Ge YX, Angenent GC, Dahlhaus E, Franken J, Peters J, Wullems GJ, Creemers-Molenaar J (2001) Partial silencing of the NEC1 gene results in early opening of anthers in Petunia hybrida. Mol Genet Genomics 265:414–423
Gorguet B, Schipper D, van Lammeren A, Visser RG, van Heusden AW (2009) Ps-2, the gene responsible for functional sterility in tomato, due to non-dehiscent anthers, is the result of a mutation in a novel polygalacturonase gene. Theor Appl Genet 118:1199–1209
Guan K, Dixon JE (1991) Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal Biochem 192:262–267
Han MJ, Jung KH, Yi G, Lee DY, An G (2007) Rice Immature Pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 48:204
Heslop-Harrison Y, Heslop-Harrison JS (1996) Lodicule function and filament extension in the grasses: potassium ion movement and tissue specialization. Ann Bot 77:573–582
Ichimura KAZU, Suto KENI (1998) Environmental factors controlling flower opening and closing in a Portulaca Hybrid. Ann Bot 82:67–70
Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209
Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31
Keijzer CJ (1987) The processes of anther dehiscence and pollen dispersal. I. The opening mechanism of longitudinally dehiscing anthers. New Phytol 105:487–498
Kombrink E (2012) Chemical and genetic exploration of jasmonate biosynthesis and signaling paths. Planta 236:1351–1366
Koo AJ, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-l-isoleucine. Proc Nat Acad Sci USA 108:9298–9303
Kramell R, Porzel A, Miersch O, Schneider G (1999) Analysis of synthetic isoleucine conjugates of cucurbic acid isomers by liquid chromatography. Phytochem Anal 10:82–87
Matsui T, Omasa K, Horie T (1999) Mechanism of anther dehiscence in rice (Oryza sativa L.). Ann Bot 84:501–506
Matsuo T, Hoshikawa K (1993) Science of the rice plant. Rural Culture Association, Tokyo, pp 341–345
McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8:403–416
McElroy D, Rothenberg M, Wu R (1990) Structural characterization of a rice actin gene. Plant Mol Biol 14:163–171
Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006
Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against Insertion in retrotransposon-rich regions of the genome. Plant Cell 15:1771–1780
Ogawa M, Kay P, Wilson S, Swain SM (2009) Arabidopsis DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21:216–233
Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31:1–12
Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089–3100
Qin Y, Yang J, Zhao J (2005) Calcium changes and the response to methyl jasmonate in rice lodicules during anthesis. Protoplasma 225:103–112
Riemann M, Takano M (2008) Rice JASMONATE RESISTANT 1 is involved in phytochrome and jasmonate signalling. Plant Cell Environ 31:783–792
Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12:1041–1062
Scarpella E, Rueb S, Boot KJ, Hoge JHC, Meijer AH (2000) A role for the rice homeobox gene Oshox1 in provascular cell fate commitment. Development 127:3655–3669
Schuller A, Ludwig-Muller J (2006) A family of auxin conjugate hydrolases from Brassica rapa: characterization and expression during clubroot disease. New Phytol 171:145–157
Senatore A, Trobacher CP, Greenwood JS (2009) Ricinosomes predict programmed cell death leading to anther dehiscence in tomato. Plant Physiol 149:775–790
Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D (2011) The jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23:1000–1013
Staswick PE (2009) The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol 150:1310–1321
Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127
Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627
Steiner-Lange S, Unte US, Eckstein L, Yang C, Wilson ZA, Schmelzer E, Dekker K, Saedler H (2003) Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J 34:519–528
Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97:10625–10630
Suza WP, Staswick PE (2008) The role of JAR1 in Jasmonoyl-l-isoleucine production during Arabidopsis wound response. Planta 227:1221–1232
Suza WP, Rowe ML, Hamberg M, Staswick PE (2010) A tomato enzyme synthesizes (+)-7-iso-jasmonoyl-l-isoleucine in wounded leaves. Planta 231:717–728
Svyatyna K, Jikumaru Y, Brendel R, Reichelt M, Mithofer A, Takano M, Kamiya Y, Nick P, Riemann M (2014) Light induces jasmonate-isoleucine conjugation via OsJAR1-dependent and -independent pathways in rice. Plant Cell Environ 37:827–839
Tabata R, Ikezaki M, Fujibe T, Aida M, Tian CE, Ueno Y, Yamamoto KT, Machida Y, Nakamura K, Ishiguro S (2010) Arabidopsis auxin response factor6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol 51:164–175
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665
Von Malek B, van der Graaff E, Schneitz K, Keller B (2002) The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216:187–192
Wakuta S, Suzuki E, Saburi W, Matsuura H, Nabeta K, Imai R, Matsui H (2011) OsJAR1 and OsJAR2 are jasmonyl-l-isoleucine synthases involved in wound—and pathogen-induced jasmonic acid signalling. Biochem Biophys Res Commun 409:634–639
Wang Y, Kumar PP (2007) Characterization of two ethylene receptors PhERS1 and PhETR2 from petunia: PhETR2 regulates timing of anther dehiscence. J Exp Bot 58:533–544
Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094
Yang C, Xu Z, Song J, Conner K, Barrena GV, Wilson ZA (2007) Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. Plant Cell 19:534–548
Zeng X, Zhou X, Zhang W, Murofushi N, Kitahara T, Kamuro Y (1999) Opening of rice floret in rapid response to methyl jasmonate. J Plant Growth Regul 18:153–158
Zhong W, Yunjie G, Yuzhu G (1991) Studies on the mechanism of the anthesis of rice III. Structure of the lodicule and changes of its contents during flowering. Acta Agron Sin 17:96–101
Zhu QH, Ramm K, Shivakkumar R, Dennis ES, Upadhyaya NM (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiol 135:1514–1525
Acknowledgments
The Tos17 lines used in this work were developed by Drs. Akio Miyao and Hirohiko Hirochika (Miyao et al. 2003) and were provided by the Rice Genome Resource Center (Tsukuba, Japan). We are grateful to Gerda Lamers for her technical support in microscopy. We thank Ward de Winter for tissue culture media and Elly Schrijnemakers for plant caretaking. This research was supported by the Programme for Strategic Scientific Alliances (04-PSA-BD-04) between China and the Netherlands of the Royal Netherlands Academy of Arts and Sciences (KNAW) for MW, PBFO, YX, ZZ and the KNAW China Exchange Programme (KNAW-CEP 04CDP022, 06CDO033, 07CDP005, 08CDP042) for YX and YC. We acknowledge financial support from the Netherlands Organization for Scientific Research (NWO; VICI-grant) to HJB, TC and PPJM.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Yuguo Xiao and Yi Chen have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xiao, Y., Chen, Y., Charnikhova, T. et al. OsJAR1 is required for JA-regulated floret opening and anther dehiscence in rice. Plant Mol Biol 86, 19–33 (2014). https://doi.org/10.1007/s11103-014-0212-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-014-0212-y