Cold‐induced repression of the rice anther‐specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility

Abstract

Low temperatures during rice ( Oryza sativa L.) pollen development cause pollen sterility and decreased grain yield. We show that the time of highest sensitivity to cold coincides with the time of peak tapetal activity: the transition of the tetrad to early uni-nucleate stage (young microspore, YM stage). Low temperatures at this stage of pollen development result in an accumulation of sucrose in the anthers, accompanied by decreased activity of cell wall bound acid invertase and depletion of starch in mature pollen grains. Expression analysis of two cell wall ( OSINV1, 4 ) and one vacuolar ( OSINV2 ) acid invertase genes showed that OSINV4 is anther-specific and downregulated by cold treatment. OSINV4 is transiently expressed in the tapetum cell layer at the YM stage, and later from the early binucleate stage in the maturing microspores. The down-regulation of OSINV4 expression in the tapetum at YM may cause a disruption in hexose production and starch formation in the pollen grains. In a cold-tolerant cultivar, OSINV4 expression was not reduced by cold; sucrose did not accumulate in the anthers and starch formation in the pollen grains was not affected.

Sensitivity of flowering plant gametophytes to temperature fluctuations

“…Intra-specific variability has indeed been extensively reported in cultivated plant species for many reproductive characteristics. Genotype-specific responses have been reported for stress applied during microsporogenesis affecting carbohydrate metabolism, degeneration of the tapetal tissues, pollen wall architecture, pollen morphology, pollen viability, anther dehiscence and pollen production (Aloni et al, 2001;Koti et al, 2005;Oliver et al, 2005;Porch and Jahn, 2001;Prasad et al, 2006;Pressman et al, 2002;Srinivasan et al, 1999;Suzuki et al, 2001). At the post-anthesis level, pollen germination (Hedhly et al, 2005a;Kakani et al, 2002Kakani et al, , 2005, pollen tube growth rate (Clarke and Siddique, 2004;Hedhly et al, 2004;Srinivasan et al, 1999), and pollen dynamics (Hedhly et al, 2005a) also show genotype-specific responses.…”

“…cell wall and vacuolar invertase, sucrose synthase) and transport, are gaining higher research interest as indicators of losses in pollen viability due to temperature fluctuations. Both cold (Oliver et al, 2005) and heat stress (Pressman et al, 2006;Sato et al, 2006) have been shown to down regulate gene expression of several invertase and sucrose synthase isomorphs, and this inhibition was accompanied by a disruption of sucrose and starch…”

“…A c c e p t e d M a n u s c r i p t 9 turnover in developing pollen grains, and, hence, lower accumulation of soluble carbohydrates (Aloni et al, 1991;Jain et al, 2007;Oliver et al, 2005;Pressman et al, 2002;Sato et al, 2002). A complete understanding of temperature stress on pollen development must await further understanding of carbohydrate turnover during this phase.…”

A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa L.)

“…heat stressed pistil pollinated with fresh pollen and vice versa wherein female reproductive organ did not reduce fertility even with 40 C exposure, whereas pollen exposed to 38 C led to a significant decline in spikelet fertility (Yoshida et al 1981). Further, the majority of the physiological or molecular studies dealing with microsporogenesis have drawn conclusions based on a single genotype (Kerim et al 2003;Hobo et al 2008;Oliver et al 2005Oliver et al , 2007Endo et al 2009). We hypothesise that spikelet size (length) coinciding with microsporogenesis varies with genotypes.…”

“…Microsporogenesis, the highly sensitive stage to heat stress (Matsui et al 2000), has not been studied extensively due to the lack of a precise phenotypic marker. However, a marker based on inter auricle distance has been identified for cold stress phenotyping (Satake and Hayase 1970), and extended to quantify the impact of cold (Oliver et al 2005(Oliver et al , 2007 and drought stress (Ji et al 2010;Liu and Bennett 2011) during young microspore and bi-nucleate pollen stages. The classic work by Satake and Hayase (1970) used different inter auricle distances and stress exposure duration to examine just two contrasting rice entries, indicating the challenge in identifying a robust marker that could be used across many genotypes.…”