Sugar and Auxin Signaling Pathways Respond to High-Temperature Stress during Anther Development as Revealed by Transcript Profiling Analysis in Cotton  

Abstract

Male reproduction in flowering plants is highly sensitive to high temperature (HT). To investigate molecular mechanisms of the response of cotton (Gossypium hirsutum) anthers to HT, a relatively complete comparative transcriptome analysis was performed during anther development of cotton lines 84021 and H05 under normal temperature and HT conditions. In total, 4,599 differentially expressed genes were screened; the differentially expressed genes were mainly related to epigenetic modifications, carbohydrate metabolism, and plant hormone signaling. Detailed studies showed that the deficiency in S-ADENOSYL-L-HOMOCYSTEINE HYDROLASE1 and the inhibition of methyltransferases contributed to genome-wide hypomethylation in H05, and the increased expression of histone constitution genes contributed to DNA stability in 84021. Furthermore, HT induced the expression of CASEIN KINASEI (GhCKI) in H05, coupled with the suppression of starch synthase activity, decreases in glucose level during anther development, and increases in indole-3-acetic acid (IAA) level in late-stage anthers. The same changes also were observed in Arabidopsis (Arabidopsis thaliana) GhCKI overexpression lines. These results suggest that GhCKI, sugar, and auxin may be key regulators of the anther response to HT stress. Moreover, PHYTOCHROME-INTERACTING FACTOR genes (PIFs), which are involved in linking sugar and auxin and are regulated by sugar, might positively regulate IAA biosynthesis in the cotton anther response to HT. Additionally, exogenous IAA application revealed that high background IAA may be a disadvantage for latestage cotton anthers during HT stress. Overall, the linking of HT, sugar, PIFs, and IAA, together with our previously reported data on GhCKI, may provide dynamic coordination of plant anther responses to HT stress.

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

“…Microscopic confirmation of abortion at this stage following exposure to temperatures ≥30 • C has been reported for cereal and eudicot crops to include rice ( Fig. 3D; Bagha, 2014), wheat (Saini and Aspinall, 1982;Saini et al, 1984), sorghum (Jain et al, 2007), barley (Sakata et al, 2000;Oshino et al, 2007), snap beans (Suzuki et al, 2001), cowpea (Ahmed et al, 1992), tomato (Iwahori, 1965), Brachypodium distachyon (Harsant et al, 2013), cotton (Min et al, 2014), and garlic (Mayer et al, 2015). The uninucleate stage is more sensitive in the low 30 • C range in cool-season crops such as barley, wheat, and garlic whereas temperatures in the mid-to-upper 30 • C range effect development in warm-season crops.…”

“…The negative impact of HT and other stresses on the timing of tapetal cell death and tapetal invertase activity is proposed to limit provisioning of compounds, to include hexose, to developing pollen and it has been hypothesized that this results in microspore starvation and subsequently, abortion (Parish et al, 2012;De Storme and Geelen, 2014). Mistimed tapetum programmed cell death or downregulation of invertase genes are not universally associated with abortion of uninucleate microspores at HT (Endo et al, 2009;Bagha, 2014;Min et al, 2014). Alterations in tapetal death and carbohydrate metabolism in anthers following exposure to HT, to include invertase activity in some species, may be only part of a complex response wherein a network that normally senses elevated temperatures and re-establishes cellular homeostasis subsequently fails.…”

Critical Roles of Vacuolar Invertase in Floral Organ Development and Male and Female Fertilities Are Revealed through Characterization of GhVIN1-RNAi Cotton Plants

“…This, together with recent progress on the roles of sugars in auxin biosynthesis and signaling (Wang and Ruan, 2013), prompted us to investigate the expression of auxin-related genes in 21-d stamen. Several stamen-expressed candidate genes involved in auxin biosynthesis, transport, and perception were chosen to measure their mRNA levels, based on previous studies (Min et al, 2014). Most notably, the transcripts of two auxin biosynthesis genes, GhTAA1 and GhYUC5, were reduced significantly in the RNAi stamen (Fig.…”

“…For example, heat-stressed cotton plants also exhibit abnormal stigma protrusion, delayed anther dehiscence, and reduced pollen viability (Brown, 2001;Snider et al, 2009;Min et al, 2014) as well as high rates of boll shedding and seed abortion (Powell, 1969;Reddy et al, 1992;Brown, 2001). Min et al (2014) also reported that the impaired anther and pollen development under high temperature were associated with reduced expression of INV and starch synthesis genes, decreased Glc level, as well as disrupted auxin biosynthesis. Similarly, wheat male reproductive failure under water deficit was related to decreased VIN (Ivr5) and CWIN (Ivr1) gene expression in pollen (Koonjul et al, 2005).…”

LEAFY COTYLEDON1-CASEIN KINASE I-TCP15-PHYTOCHROME INTERACTING FACTOR4 Network Regulates Somatic Embryogenesis by Regulating Auxin Homeostasis

“…To evaluate the potential production of EC, cotton explants that were transformed with 35S::GUS, 35S: GhCKI, and 35S:iGhCKIv, callus of transgenic Arabidopsis plants, and mutant lines from different culture times were imaged using a Nikon D40 Camera. The cotton explants were sectioned into 8-mm-thick slices with a microtome, stained with 0.1% aniline blue, and observed according to the work by Min et al (2014). Electronic microscopic analyses (TEM) of the callus were conducted as previously described (Min et al, 2013).…”