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

Abstract

Abstract. Gametogenesis in rice (Oryza sativa L.), and particularly male gametogenesis, is a critical developmental stage affected by different abiotic stresses. Research on this stage is limited, as flowering stage has been the major focus for research to date. Our main objective was to identify a phenotypic marker for male gametogenesis and the duration of exposure needed to quantify the impact of heat stress at this stage. Spikelet size coinciding with microsporogenesis was identified using parafilm sectioning, and the panicle (spikelet) growth rate was established. The environmental stability of the marker was ascertained with different nitrogen (75 and 125 kg ha -1 ) and night temperature (22 C and 28 C) combinations under field conditions. A distance of -8 to -9 cm between the collar of the last fully opened leaf and the flag leaf collar, which was yet to emerge was identified as the environmentally stable phenotypic marker. Heat stress (38 C) imposed using the identified marker induced 8-63% spikelet sterility across seven genetically diverse rice genotypes. Identifying the right stage based on the marker information and imposing 6 consecutive days of heat stress ensures that >95% of the spikelets in a panicle are stressed spanning across the entire microsporogenesis stage.

The effect of high temperature stress on male and female reproduction in plants

“…Studies assessing the cellular and developmental aspects of anther/pollen development and the influence of HT on these parameters do so in the context of anther length (Raghavan, 1988;Hill, 1996;Harsant et al, 2013), and Alexander's triple stain has been used as a rapid and effective way to stage pollen development as a function of anther length (Harsant et al, 2013). Other investigators use floral bud length as a proxy for anther/pollen development (Giorno et al, 2013;Smyth et al, 1990), the 'days-before-anthesis' as a guide for predicting the stages of anther/pollen development (Satake and Yoshida, 1978;Sakata et al, 2000;Jain et al, 2007;Giorno et al, 2013) or other phenotypic markers (Jagadish et al, 2014). The most important information from these types of studies is that anther development within a flower can span up to two weeks in wheat and tomato (Saini and Aspinall, 1982;Giorno et al, 2013), nine days in rice (Satake and Yoshida, 1978), and a week in barley and sorghum (Sakata et al, 2000;Jain et al, 2007).…”

“…Air and tissue temperatures >30 • C prior to anther opening can severely delay or prevent anther dehiscence in tomato, rice, and Brachypodium (Rudich et al, 1977;Matsui et al, 2001;Porch and Jahn, 2001;Saini and Aspinall, 1982;Jagadish et al, 2007Jagadish et al, , 2010Jagadish et al, , 2014Harsant et al, 2013;Maruyama et al, 2013;Min et al, 2013;Song et al, 2015). A minimum number of pollen grains are required for fertilization because of pollen tube attrition during growth en route to ovules (Erbar, 2003).…”

Acquired Thermo‐Tolerance and Trans‐Generational Heat Stress Response at Flowering in Rice

“…Similarly, 4 days of heat stress coinciding with gametogenesis stage resulted in significant reduction in pollen viability and spikelet fertility (Jagadish et al. ). The impact of heat stress coinciding with the gametogenesis and flowering is known to be irreversible, and hence, extending stress period for longer duration would still have the same impact as the short episodes of exposure coinciding with the critical stages.…”

Effective Strategies for Enhancing Tolerance to High-Temperature Stress in Rice during the Reproductive and Ripening Stages

“…Pollen tends to be more sensitive than the female gametophyte to HTS across plant species, including chickpea (Cicer arietinum) (Clarke and Siddique 2004;Devasirvatham et al 2012Devasirvatham et al , 2013Kaushal et al 2013), rice (Sakata and Higashitani 2008;Wassmann et al 2009), tomato (Lycopersicon esculentum) (Giorno et al 2013), maize (Zea mays) (Herrero and Johnson 1980), and Vigna unguiculata (Ahmed et al 1992). When compared with other cereal crops such as maize and wheat (Triticum aestivum), rice is relatively more sensitive to HTS (＞ 35°C), mainly during the stages of flowering (Prasad et al 2006;Jagadish et al 2007Jagadish et al , 2008Jagadish et al , 2010b and gametogenesis (Jagadish et al 2013). Under such high temperatures, microspores are aborted and pollen viability is reduced during anthesis, subsequently causing spikelet sterility (Cheng et al 2009;Mohammed and Tarpley 2009a, 2009b.…”

“…Rice plants are most sensitive to high temperatures at the reproductive (anthesis) stage (Yoshida et al 1981), and frequent increases in temperature above the critical level of 33°C result in spikelet sterility and serious losses in grain yields (Nakagawa et al 2002). Therefore, the rice reproductive organs can be severely affected by HTS depending upon the duration and the extent of the stress (Wahid et al 2007;Jagadish et al 2013).…”