High Temperatures Cause Male Sterility in Rice Plants with Transcriptional Alterations During Pollen Development

Abstract

Plant male reproductive development is highly organized and sensitive to various environmental stressors, including high temperature. We have established an experimental procedure to evaluate high temperature injury in japonica rice plants. High temperature treatment (39 degrees C/30 degrees C) starting at the microspore stage repeatedly reduced spikelet fertility in our system. Morphological observations revealed that pollen viability in plants exposed to high temperatures was lower than that in control plants. Most pollen grains in high temperature-treated plants displayed a normal round shape and stained reddish purple with Alexander's reagent; however, the pollen grains were very poorly attached and displayed limited germination on the stigma. To investigate gene regulatory mechanisms in the anther in high temperature environments, DNA microarray analysis was performed by comparing non-treated samples with samples treated with 2-4 d of high heat. Genes responsive to high temperatures were identified from clustering of microarray data. Among these, at least 13 were designated as high temperature-repressed genes in the anther. Expression analyses revealed that these genes were expressed specifically in the immature anther mainly in the tapetum at the microspore stage and down-regulated after 1 d of high temperature. The expression levels of Osc6, OsRAFTIN and TDR, which are tapetum-specific genes, were unaffected by high temperatures. These results suggest that not all tapetal genes are inhibited by increased temperatures and the tapetum itself is not degraded in such an environment. However, high temperatures may disrupt some of the tapetum functions required for pollen adhesion and germination on the stigma.

Responses of spikelet fertility to air, spikelet, and panicle temperatures and vapor pressure deficit in rice

“…Dehisced thecae and length of basal dehiscence were highly related to the number of swelling pollen (Matsui et al, 2002;Kobayasi et al, 2011). Therefore, these processes resulted in low number of germinating pollen grains on the stigma which was well known as main cause of male sterility in high temperature condition (Satake and Yoshida, 1978;Matsui et al, 2000;Matsui et al, 2001;Jagadish et al, 2007;Endo et al, 2009;Jagadish et al, 2011;Shah et al, 2011). Pollen which was exposed to high temperature condition could be viable as short as 10 minutes (Song et al, 2001), and the proportion of germinated pollen also was reduced under high temperature condition (Jagadish et al, 2010).…”

Arabidopsis Pollen Fertility Requires the Transcription Factors CITF1 and SPL7 That Regulate Copper Delivery to Anthers and Jasmonic Acid Synthesis

“…In addition to being controlled by Cu availability and other environmental factors (Endo et al, 2009;Smith and Zhao, 2016;Broadley et al, 2012), plant reproduction, including male fertility, is regulated by hormonal cues (Yuan and Zhang, 2015;Cheng et al, 2004;Cecchetti et al, 2008;Song et al, 2013). In this regard, jasmonic acid (JA) and related jasmonate metabolites, collectively called jasmonates, are lipid-derived signaling compounds that in addition to their well established role in plant responses to biotic and abiotic stresses, regulate stamen development and male fertility (Browse, 2009).…”

Genome-Wide Association Mapping of Fertility Reduction upon Heat Stress Reveals Developmental Stage-Specific QTLs in Arabidopsis thaliana

“…Heat stress also leads to shortening of the anthers, due to a reduced amount of auxin (Sakata et al, 2010), which results in a mismatch between the ripening of the stigma and anthers, preventing self-fertilization in bisexual monoecious plants. Moreover, viability of pollen is reduced by disruption of male meiosis upon heat stress (Endo et al, 2009). In addition to disturbance of the development of male organs and pollen, changes in the development of the female organs have also been reported.…”