Rice SIZ1, a SUMO E3 ligase, controls spikelet fertility through regulation of anther dehiscence

Abstract

Summary• Sumoylation, a post-translational modification, has important functions in both animals and plants. However, the biological function of the SUMO E3 ligase, SIZ1, in rice (Oryza sativa) is still under investigation.• In this study, we employed two different genetic approaches, the use of siz1 T-DNA mutant and SIZ1-RNAi transgenic plants, to characterize the function of rice SIZ1.• Genetic results revealed the co-segregation of single T-DNA insertional recessive mutation with the observed phenotypes in siz1. In addition to showing reduced plant height, tiller number and seed set percentage, both the siz1 mutant and SIZ1-RNAi transgenic plants showed obvious defects in anther dehiscence, but not pollen viability. The anther indehiscence in siz1 was probably a result of defects in endothecium development before anthesis. Interestingly, rice orthologs of AtIRX and ZmMADS2, which are essential for endothecium development during anther dehiscence, were significantly down-regulated in siz1. Compared with the wild-type, the sumoylation profile of high-molecular-weight proteins in mature spikelets was reduced significantly in siz1 and the SIZ1-RNAi line with notably reduced SIZ1 expression. The nuclear localization signal located in the SIZ1 C-terminus was sufficient for its nuclear targeting in bombarded onion epidermis.• The results suggest the functional role of SIZ1, a SUMO E3 ligase, in regulating rice anther dehiscence.

Defining the SUMO System in Maize: SUMOylation Is Up-Regulated during Endosperm Development and Rapidly Induced by Stress

“…A similar suppression was seen in Arabidopsis, indicating that this stress memory might be universal in terrestrial plants (Kurepa et al, 2003). The protective role of SUMO conjugation during stress also is supported by the stress-sensitive phenotypes associated with SUMO pathway loss-of-function mutants in Arabidopsis, rice, and yeast (Tanaka et al, 1999;Miura et al, 2007;Conti et al, 2008;Golebiowski et al, 2009;Chaikam and Karlson, 2010;Thangasamy et al, 2011). Less clear is how SUMO protects organisms from suboptimal growth conditions.…”

“…Previous studies with rice (Oryza sativa) showed that SUMOylation is active in growing tissues and, like that in Arabidopsis, is strongly up-regulated upon exposure to heat, cold, high salt, and abscisic acid (Chaikam and Karlson, 2010;Park et al, 2010). Rice siz1 alleles that attenuate SUMOylation have a smaller stature with a reduced root system, greater tillering, and reduced fecundity (Thangasamy et al, 2011) and accumulate higher levels of nitrogen and phosphorous, possibly due to the altered expression of genes involved in nutrient uptake (Wang et al, 2015). Conversely, OTS1 overexpression rendered rice resistant to high salt, whereas RNA interference-mediated silencing enhanced salt sensitivity (Srivastava et al, 2016).…”

Overexpression of the Rice SUMO E3 Ligase Gene OsSIZ1 in Cotton Enhances Drought and Heat Tolerance, and Substantially Improves Fiber Yields in the Field under Reduced Irrigation and Rainfed Conditions

“…The OsSIZ1 and AtSIZ1 proteins share 51% identity at the amino acid level (Park et al 2010). The SUMO E3 ligase is known to regulate various aspects of plant growth and development such as ABA signaling (Miura et al 2009), innate immunity through salicylic acid signaling (Miura and Hasegawa 2010), nitrogen assimilation (Park et al 2011), spikelet fertility in rice (Thangasamy et al 2011) and flowering (Jin et al 2008). Besides its roles in regulating plant growth and development, Arabidopsis SIZ1 was shown to play roles in stress tolerance against various environmental stresses such as low temperature stress via sumoylation and stabilization of the ICE1 transcription factor (Miura et al 2007b), heat stress (Kurepa et al 2003, Yoo et al 2006, Saracco et al 2007), water deficit stress (Catala et al 2007), phosphate starvation stress (Miura et al 2005) and metal stress such as copper stress (Chen et al 2011).…”

bHLH142 regulates various metabolic pathway-related genes to affect pollen development and anther dehiscence in rice

“…DEFECTIVE IN ANTHER DEHISCENCE1 (DAD1) gene encodes phospholipase enzyme required for jasmonic acid biosynthesis and regulates anther dehiscence in Arabidopsis. Knock-down/Knock-out of SIZ1 , a SUMO E3 ligase gene, resulted in sterile rice plant due to lack of anther dehiscence24. Pollen Semi-Sterility1 (PSS1) encodes a kinesin-like protein that regulates both pollen development and anther dehiscence process in rice25.…”