Methyl jasmonate triggers loss of grain yield under drought stress

Abstract

Drought is one of the major constraints to rice production worldwide. The development of rice panicle and spikelet meristem is repressed under the drought conditions, resulting in a reduction in the numbers of panicles and spikelets. In our recent report, we demonstrated that methyl jasmonate (MeJA) plays an important role in drought-induced loss of grain yield. Transgenic overexpression of the Arabidopsis gene jasmonic acid carboxyl methyltransferase (AtJMT) in rice resulted in a large reduction in grain yield through increased MeJA and ABA levels in young panicles. Exposure of nontransgenic plants to drought conditions also increased MeJA and ABA levels in young panicles and significantly reduced grain yield. In both cases, the reduction in grain yield was due to lower numbers of spikelets and lower filling rates than were observed for nontransgenic (NT) controls. The ABA increase in AtJMT transgenic panicles grown in non-drought conditions suggests that MeJA, rather than drought stress, induces ABA biosynthesis under drought conditions. These results led us postulate that plants produce MeJA during drought stress, which in turn stimulates the production of ABA, together leading to a loss of grain yield.

Introduction

Rice plants grow in a paddy field and, therefore, susceptible to water stress, in particular, to drought. Rice grain yield is determined by four parameters: number of panicles per plant, number of spikelets per panicle, filling rate and total grain weight. The number of panicles and spikelets is determined soon after formation of the panicle and spikelet meristems.¹ Drought exposure during the earlier stages of reproductive growth affects the first two parameters more than the other parameters, while drought exposure at later stages affects the filling rate more than the other parameters. Abscisic acid (ABA) has been implicated in a reduction of grain yield following water stress during reproductive plant development. ABA levels were increased upon exposure of plants to drought conditions, which reduces the filling rate by increasing sterility in cereal plants.^2–5 These studies focused on plant hormone levels during the late stages of reproductive development, including meiosis and/or grain filling periods following exposure to drought conditions. However, studies on plant hormone levels during the early stages of reproductive development, which determine the number of panicles and spikelets, are currently lacking. In the present study, we examined MeJA and ABA levels under drought conditions during the panicle initiation stage.⁶

Increases in MeJA and ABA Levels during Drought Stress

To study the role of MeJA in drought-induced loss of grain yield, we generated transgenic rice plants that overexpress the Arabidopsis JA carboxyl methyltransferase gene (AtJMT).⁷ The AtJMT transgenic panicles had MeJA levels that were 6-fold higher than those of nontransgenic (NT) panicles. Grain yield, number of spikelets per panicle and filling rate were also largely reduced in AtJMT plants as compared to NT controls, a typical phenomenon observed in plants exposed to drought stress. MeJA was found to be 19-fold higher in drought-treated NT panicles than in untreated NT panicles. Levels of abscisic acid (ABA), were also increased by 1.4- and 1.9-fold in the drought-treated NT and the AtJMT panicles, respectively, as compared to untreated NT panicles. In particular, the ABA increase in AtJMT transgenic panicles grown in non-drought conditions suggests that MeJA, rather than drought stress, induces ABA biosynthesis under drought conditions. Grain yield was significantly reduced in the AtJMT plants. A similar reduction in grain yield was also observed in NT plants following drought stress or treatment with exogenous MeJA at the panicle initiation stage. Together, these results suggested that MeJA triggers reduction in grain yield by affecting the development of spikelets.

MeJA Together with ABA Alter Spikelet Development during Drought Stress

Several alterations in spikelet organ numbers were noted in the developing spikelets of Ubi1:AtJMT plants. Similar alterations in spikelet organ numbers were also observed in NT plants following drought stress or treatment with exogenous MeJA at the panicle initiation stage, suggesting that increased levels of MeJA in both AtJMT transgenic and drought-treated NT plants are responsible for alteration in spikelet organ numbers. Global expression profilings performed on panicles from AtJMT transgenic, drought-treated NT and untreated NT plants led us to identify 7genes that may together mediate hormone signals to the loss of grain yield. The selected genes were regulated in both AtJMT and drought-treated NT panicles and include two genes, OsJMT1 and OsSDR, that are involved in MeJA and ABA biosynthesis, respectively.

These results led us to propose a simplified model by which plants may respond to drought stress (Fig. 1). Plants start to produce MeJA upon exposure to drought stress, which in turn stimulates the production of ABA. The OsSDR gene was upregulated in both AtJMT panicles and drought-treated NT panicles, suggesting its involvement in MeJA-dependent biosynthesis of ABA.⁸ The activity of the Arabidopsis SDR gene was reported to be required for JA biosynthesis, suggesting that ABA either precedes or cooperates with JA in signaling pathways.⁹ It is therefore possible that a positive feedback exists between MeJA and ABA under drought conditions.¹⁰ Expression of OsJMT1, a rice orthologue of AtJMT, was also increased in AtJMT transgenic and drought-treated NT panicles, indicating that OsJMT1 may be responsible for the biosynthesis of MeJA upon exposure to drought conditions. Finally, the increased levels of MeJA and ABA alter spikelet development, resulting in a loss of grain yield under drought conditions.

Figure 1.

A proposed model for a drought-induced loss of rice grain yield. Upon plant exposure to drought stress during early stages of reproductive development, developing panicles start to produce methyl jasmonate (MeJA) via increased activity of OsJMT1, a rice orthologue of AtJMT. The elevated level of MeJA stimulates both biosynthesis of abscisic acid (ABA) by activating OsSDR, an Arabidopsis orthologue of which is essential for ABA biosynthesis⁸ and expression of OsJMT1, increasing the MeJA level further. ABA biosynthesis can also be stimulated directly by drought stress, independently from MeJA. The increased levels of MeJA and ABA together alter spikelet development, resulting in a loss of grain yield under drought conditions.

Addendum to: Kim EH, Kim YS, Park S-H, Koo YJ, Choi YD, Chung Y-Y, Lee I-J, Kim J-K. Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol. 2009 doi: 10.1104/pp.108.134684. In press.