The Rice Pentatricopeptide Repeat Gene TCD10 is Needed for Chloroplast Development under Cold Stress

Abstract

BackgroundChloroplast plays a vital role in plant development and growth. The pentatricopeptide repeat (PPR) gene family is one of the largest gene families in plants. In addition, cold stress affects a broad spectrum of cellular components, e.g. chloroplast, and metabolism in plants. However, the regulatory mechanism for rice PPR genes on chloroplast development still remains elusive under cold stress.ResultIn this paper, we characterized a new rice PPR gene mutant tcd10 (thermo-sensitive chlorophyll-deficient mutant 10) that exhibits the albino phenotype, malformed chloroplast and could not survive after the 5-leaf stage when grown at 20 °C, but does the normal phenotype at 32 °C. Map-based cloning, followed by RNA interference and CRISPR/Cas9 genome editing techniques, revealed that TCD10 encoding a novel PPR protein, mainly localized to the chloroplasts, with 27 PPR motifs, is responsible for the mutant phenotype. In addition, TCD10 is specific expression in tissues. The disruption of TCD10 resulted in an evidently reduced expression of chloroplast-associated genes under cold stress (20 °C), whereas they did recovered to normal levels at high temperature (32 °C). These results showed an important role of TCD10 for chloroplast development under cold stress.ConclusionsThe TCD10 encodes a novel rice PPR protein, mainly located in chloroplasts, which is important for chloroplast development, growth and the maintenance of photosynthetic electron transport and its disorder would lead to an aberrant chloroplast and abnormal expressions in these genes for chloroplast development and photosynthesis in rice under cold stress.Electronic supplementary materialThe online version of this article (doi:10.1186/s12284-016-0134-1) contains supplementary material, which is available to authorized users.

Cold signaling in plants: Insights into mechanisms and regulation

“…Low‐temperature stress causes obvious damage to plants, including wilting, discoloration, drying of leaf edges, accelerated aging, incomplete ripening, and even death. Moreover, chlorotic leaves or albino phenotypes occur under cold‐stress conditions and the key genes, such as OsV4 ( Oryza sativa Virescent 4 ), TCD10 ( Thermo‐sensitive Chlorophyll‐deficient mutant 10 ), TCD11 ( Thermo‐sensitive Chlorophyll‐deficient mutant 11 ), TSV ( Thermo‐sensitive Virescent mutant ), and TSV3 ( Thermo‐sensitive Virescent mutant 3 ) are essential for chloroplast development at low temperatures in Arabidopsis (Gong et al ; Wu et al ; Sun et al ; Wang et al ; Lin et al ). Lateral roots are model tissues for studying the response to cold stress in Arabidopsis .…”

The RNA editing factor DUA1 is crucial to chloroplast development at low temperature in rice

“…To date, eight rice genes ( V1, V2, V3, WLP1, St1, TCD5, TCD9 and TCD10 ) have been identified as contributing to chloroplast development under low temperature. These genes influence chloroplast development, chloroplast biogenesis and chlorophyll biosynthesis (Kusumi et al ., ; Sugimoto et al ., ; Yoo et al ., ; Gong et al ., ; Song et al ., ; Y. Wang et al ., ; L. Wu et al ., ). Almost all studies of the regulation of chloroplast development have been focused at the transcriptional level, and few studies of the posttranscriptional regulation of chloroplast development under chilling stress have been performed.…”

“…However, little or no functional redundancy among PPR proteins has been found in higher plants, this situation indicates that the functions of PPR proteins are highly diversified in these plants. Accumulating evidence has revealed that PPR proteins are involved in a wide range of biological processes, such as cytoplasmic male sterility (CMS; Gaborieau et al ., ; Igarashi et al ., ; Liu et al ., , ), embryogenesis (Cai et al ., ; Li et al ., ; Tadini et al ., ), retrograde signaling (Sun et al ., ), and low temperature stress (Wu et al ., ; Wang et al ., ). However, the molecular mechanisms underlying the roles of PPR proteins in low temperature stress remain largely unknown.…”

“…These genes influence chloroplast development, chloroplast biogenesis and chlorophyll biosynthesis (Kusumi et al, 1997;Sugimoto et al, 2004;Yoo et al, 2009;Gong et al, 2014;Song et al, 2014; Y. L. Wu et al, 2016).…”

Rice TCM1 Encoding a Component of the TAC Complex is Required for Chloroplast Development under Cold Stress

“…Currently, more than 70 Chl‐deficient or chloroplast‐defective mutants in rice have been identified (for a review, see Kurata et al, 2005). Among these, the v1 , v2 , v3 , tcd9, osv4 , tcd5 , tcd10 , and tcd11 mutants (Iba et al, 1991; Kusumi et al, 1997; Sugimoto et al, 2007; Jiang et al, 2014; Gong et al, 2014; Wang et al 2016, 2017; Wu et al, 2016) were reported to have the similar phenotypes to the tcm1 mutants. It is known that the V1 gene encodes a chloroplast protein that is involved in the regulation of chloroplast RNA metabolism and is essential for chloroplast differentiation during early leaf development at low temperatures (Kusumi et al, 2011).…”