Cotton GhCKI disrupts normal male reproduction by delaying tapetum programmed cell death via inactivating starch synthase

Abstract

SUMMARYAnther infertility under high temperature (HT) conditions is a critical factor contributing to yield loss in cotton (Gossypium hirsutum). Using large-scale expression profile sequencing, we studied the effect of HT on cotton anther development. Our analysis revealed that altered carbohydrate metabolism or disrupted tapetal programmed cell death (PCD) underlie anther sterility. Expression of the Gossypium hirsutum casein kinase I (GhCKI) gene, which encodes a homolog of casein kinase I (CKI), was induced in an HT-sensitive cotton line after exposure to HT. As mammalian homologs of GhCKI are involved in inactivation of glycogen synthase and the regulation of apoptosis, GhCKI may be considered a target gene for improving anther fertility under HT conditions. Our studies suggest that GhCKI exhibits starch synthase kinase activity, increases glucose content in early-stage buds and activates the accumulation of abscisic acid, thereby disturbing the balance of reactive oxygen species and eventually disrupting tapetal PCD, leading to anther abortion or indehiscence. These results indicate that GhCKI may be a key regulator of tapetal PCD and anther dehiscence, with the potential to facilitate regulation of HT tolerance in crops.

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

“…the reduction of Glc content in anthers (Min et al, 2013). These results indicated that sugar homeostasis, especially the decrease in Glc content in anthers, correlated for anther abortion in H05 under HT.…”

“…However, the mechanism of bud shedding under HT is unknown. Based on our previous research, the expression of GhCKI was induced earlier in anthers by HT, which regulated anther abortion and caused bud shedding (Min et al, 2013). To globally identify the genes and pathways participating in cotton anther development under HT, we chose two cotton lines (the HT-tolerant 84021 and the HT-sensitive H05), two temperature regimes (NT, 28°C-35°C/20°C-28°C day/night; HT, 35°C-39°C/29°C-31°C day/night), and three anther development stages (TS, TDS, and ADS), corresponding to crucial stages at which male reproductive organs are sensitive to stresses (Sato et al, 2002;Endo et al, 2009).…”

“…First, decreased levels of Glc in H05 under HT (Fig. 4D) and in the GhCKI overexpressor line (Min et al, 2013) were detected. Second, the IAA content in H05 anthers was measured under two conditions (Fig.…”

“…OE25-6, with moderate GhCKI expression, exhibited normal anther dehiscence, similar to the wild type. OE15-7, with high GhCKI expression, was unable to dehisce and release pollen grains (Min et al, 2013). FW, Fresh weight.…”

“…sugar signaling and plant hormone signaling) to establish a new steadystate balance of metabolic processes by altering the composition of certain transcripts, proteins, metabolites, and lipids (McClung and Davis, 2010;Suzuki et al, 2012). In our previous study, HT induced CASEIN KINASEI (GhCKI) expression earlier in an HT-sensitive cotton line, and overexpression of GhCKI regulated anther abortion by inhibiting the activities of starch synthases, disrupting the homeostasis of Glc, abscisic acid (ABA), and reactive oxygen species and causing male sterility (Min et al, 2013). In the last 2 years, many reports have demonstrated that PHYTOCHROME-INTERACTING FACTOR genes (PIFs) were required for hypocotyl elongation at HT by regulating auxin biosynthesis (Franklin et al, 2011).…”