Effects of chilling on male gametophyte development in rice

Abstract

Chilling during male gametophyte development in rice inhibits development of microspores, causing male sterility. Changes in cellular ultrastructure that have been exposed to mild chilling include microspores with poor pollen wall formation, abnormal vacuolation and hypertrophy of the tapetum and unusual starch accumulation in the plastids of the endothecium in post-meiotic anthers. Anthers observed during tetrad release also have callose (1,3-beta-glucan) wall abnormalities as shown by immunocytochemical labelling. Expression of rice anther specific monosaccharide transporter (OsMST8) is greatly affected by chilling treatment. Perturbed carbohydrate metabolism, which is particularly triggered by repressed genes OsINV4 and OsMST8 during chilling, causes unusual starch storage in the endothecium and this also contributes to other symptoms such as vacuolation and poor microspore wall formation. Premature callose breakdown apparently restricts the basic framework of the future pollen wall. Vacuolation and hypertrophy are also symptoms of osmotic imbalance triggered by the reabsorption of callose breakdown products due to absence of OsMST8 activity.

Analysis of Sugar Content and Expression of Sucrose Transporter Genes (<i>OsSUTs</i>) in Rice Tissues in Response to a Chilling Temperature

“…On the other hand, microarray analysis of rice anthers showed that the expression of an invertase and two sucrose synthase genes was down-regulated by chilling (Yamaguchi et al 2004). It has also been reported that the expression of OsINV4 and OsMST8 (anther-specific genes) decreased in rice exposed to low temperatures, and that the decrease in the expression of OsINV4 and OsMST8 during chilling was associated with poor pollen wall formation, abnormal vacuolation and hypertrophy of the tapetum, and unusual starch accumulation in post-meiotic anthers (Mamun et al 2006, Oliver et al 2005, 2007. Thus, the changes in expression of OsSUT1, OsSUT2 and OsSUT4 accompanied by other genes related to sugar transport (Lemoine et al 2013) should cause the repression in sugar supply to the anther/pollen via long-and short-distance sucrose transport from source tissues during chilling.…”

Sensitivity of flowering plant gametophytes to temperature fluctuations

“…Special mention must be given to the work done in rice (Oryza sativa L.), initiated in the 1970s by Japanese researchers (Nishiyama, 1984;Satake and Hayase, 1970) and later confirmed by many authors (e.g. Jagadish et al, 2007;Mamun et al, 2006;Prasad et al, 2006), relating chilling and heat stress during booting (early gametophyte development) and flowering to higher spikelet sterility. Similarly, the effect of high temperatures during flowering in tomato (Solanum lycopersicum L.) has also been studied in detail, and not only extreme high temperatures, but even a mild increase in temperature during a short spell coincident with some flowering stages have been shown to affect negatively fruit set Page 6 of 24 A c c e p t e d M a n u s c r i p t 6 (Abdulbaki and Stommel, 1995;Sato et al, 2002).…”

“…Meiosis has been recurrently reported as a highly sensitive stage to temperature in many species (Ahmed et al, 1992;Clarke and Siddique, 2004;Erickson and Markhart, 2002;Prasad et al, 2003), although the precise mechanism underlying this sensitivity is still not well known. Premature dissolution of the callose wall that surrounds dividing microspores (late meiosis) and the subsequent poor wall development in the resultant microspores has been interpreted as the main reason for pollen sterility in rice under cold stress (Mamun et al, 2006). Early microspore development was reported to be also highly sensitive to chilling stress in the same species (Mamun et al, 2006).…”

“…Premature dissolution of the callose wall that surrounds dividing microspores (late meiosis) and the subsequent poor wall development in the resultant microspores has been interpreted as the main reason for pollen sterility in rice under cold stress (Mamun et al, 2006). Early microspore development was reported to be also highly sensitive to chilling stress in the same species (Mamun et al, 2006). Tapetum -the innermost layer of the anther wall-hypertrophy in rice (Nishiyama, 1984) and its earlier degeneration in many other species (Ahmed et al, 1992;Erickson and Markhart, 2002;Porch and Jahn, 2001), which deprives developing pollen grains from essential nutrients and metabolites, is another symptom frequently reported as accompanying pollen sterility under low and high temperature stresses.…”

Quantitative Trait Loci and Crop Performance under Abiotic Stress: Where Do We Stand?: Table I.

“…Excessive heat perturbs many cellular and developmental processes and directly affects grain production by reducing fertility and grain quality (Barnabás et al, 2008). Male gametophyte development is the facet of reproduction that appears most prone to disruption by drought, heat, and cold stresses (Saini, 1997;Mamun et al, 2006). However, it is unclear at present whether there is any common basis to the sensitivity of male reproduction to the various stresses.…”