A novel rice protein family of OsHIGDs may be involved in early signalling of hypoxia-promoted stem growth in deepwater rice

Abstract

OsHIGDs was identified as a novel hypoxia-responsive protein family. Among them, OsHIGD2 is characterized as a mitochondrial protein and is related to hypoxia signalling through interacting with mitochondrial proteins of critical functions in reducing cell damages caused by hypoxia. Recent evidence supports ethylene as a key factor in modulating plant responses to submergence stress. Meanwhile, there has been general consent that ethylene is not the only signal for the submergence-induced stem growth. In this study, we confirmed that hypoxia also promotes stem elongation in deepwater rice even in the absence of ethylene. As components of ethylene-independent hypoxia signalling, five HIGD (hypoxia-induced gene domain) protein genes were identified. Among the genes, OsHIGD2 showed the fastest and strongest induction by hypoxia as well as submergence. Co-expression analysis indicated that OsHIGD2 had a simultaneous expression pattern with fermentation-related genes, such as ADH1 (alcohol dehydrogenase 1) and PDC2 (pyruvate decarboxylase 2). Transient expression of OsHIGD2 in leaf epidermal cells of Nicotiana benthamiana provided evidence that the protein is localized to mitochondria. We further identified OsHIGD2-interacting proteins through the yeast two-hybrid assay using OsHIGD2 as bait. As a result, three mitochondrial proteins were discovered that function in the regulation of redox potential or reduction of protein damages caused by reactive oxygen species. In this report, we propose that OsHIGD2 is a mitochondrial protein which takes part in the early stage of hypoxia signalling by interacting with proteins that are related to oxygen utilization.

A novel approach to investigate hypoxic microenvironment during rice colonization by Magnaporthe oryzae

“…OsHIGDs, hypoxia‐induced gene domain proteins, are a novel hypoxia‐responsive protein family as components of ethylene‐independent hypoxia signalling. OsHIGD2 as a mitochondrial protein takes part in the early stage of hypoxia signalling by interacting with proteins related to oxygen utilization (Hwang and Choi, ). WRKY62, a WRKY transcription factor, positively regulates defence genes and hypoxia genes including ADH2 , Acyl desaturase and ERF068 (Fukushima et al ., ).…”

“…Nine genes responsive to hypoxia or submergence, OsCIPK15 , ADH1 (Lee et al ., ; Narsai et al ., ), OsHIGD2 , OsHIGD3 , OsHIGD5 (Hwang and Choi, ), WRKY62 , ADH2 , Acyl desaturase and ERF068 (Fukushima et al ., ), were up‐regulated during fungal infection compared to a pre‐penetration stage. Typical hypoxia genes, ADH2 involved in anaerobic glycolysis and ATP production, Acyl desaturase and ERF068 (Fukushima et al ., ), and recently reported hypoxia gene, OsHIGD2 (Hwang and Choi, ), were highly up‐regulated during the entire infection stages. This would be connected with the observations that hypoxia occurs within rice cells and tissues during fungal infection.…”

Identification and Regulation of Hypoxia-Tolerant and Germination-Related Genes in Rice

“…Recently, it was found that ethylene plays a crucial role in flooding response and metabolic acclimatization of rice, and ethylene improves rice survival at the seedling stage by enhancing specific transcription factors (VII ethylene response factors), probably by inducing autophagy and reactive oxygen species (ROS) production [23]. In recent years, more and more QTLs and candidate genes for hypoxic germination tolerance have been discovered and cloned, such as OsTPP7, OsHIGD2, and Sub1 [24][25][26][27][28][29][30][31][32][33][34]. Therefore, understanding the genes/QTL affecting rice seed germination and emergence under hypoxia stress and their roles in the mechanisms of each pathway lays the foundation for further research on the selection and improvement of hypoxia-tolerant varieties of rice, broadens the mindset, and solves difficult problems.…”

Genome-wide analysis of soybean hypoxia inducible gene domain containing genes: a functional investigation of GmHIGD3

“…The HIGD gene family has been identified in both Arabidopsis and rice plants. In rice, there are five HIGD genes: OsHIGD2 , OsHIGD3 and OsHIGD5 respond to submergence, hypoxia, and ethylene at different time points, while OsHIGD1 and OsHIGD4 exhibit almost undetectable expression under all conditions ( Hwang and Choi, 2016 ). In Arabidopsis , AtHIGD1 expression levels are induced by hypoxia treatment, and overexpression of the AtHIGD1 gene has been shown to enhance survival rates after hypoxia stress compared to wild-type plants ( Hwang et al., 2017 ).…”

“…In Arabidopsis , AtHIGD1 expression levels are induced by hypoxia treatment, and overexpression of the AtHIGD1 gene has been shown to enhance survival rates after hypoxia stress compared to wild-type plants ( Hwang et al., 2017 ). Both OsHIGD2 and AtHIGD1 localize to mitochondria ( Hwang and Choi, 2016 ; Hwang et al., 2017 ). However, no information is available on the hypoxia response information of the soybean HIGD family.…”