The rice OsV4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress

Abstract

Pentatricopeptide repeat (PPR) proteins, characterized by tandem arrays of a 35 amino acid motif, have been suggested to play central and broad roles in modulating the expression of organelle genes in plants. However, the molecular mechanisms of most rice PPR genes remains unclear. In this paper, we isolated and characterized a temperature-conditional virescent mutant, OsV4, in rice (Oryza sativa cultivar Jiahua1 (WT, japonica rice variety)). The mutant displays albino phenotype and abnormal chloroplasts at the three leaf stage, which gradually turns green after the four leaf stage at a low temperature (20 °C). But the mutant always develops green leaves and well-developed chloroplasts at a high temperature (32 °C). Genetic and molecular analyses uncovered that OsV4 encodes a novel chloroplast-targeted PPR protein including four PPR motifs. Further investigations show that the mutant phenotype is associated with changes in chlorophyll content and chloroplast development. The OsV4 transcripts only accumulate to high levels in young leaves, indicating that its expression is tissue-specific. In addition, transcript levels of some ribosomal components and plastid-encoded polymerase-dependent genes are dramatically reduced in the albino mutants grown at 20 °C. These findings suggest that OsV4 plays an important role during early chloroplast development under cold stress in rice.

Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

“…1E). Unlike other albino or chlorotic leaf mutants, whose defect in leaf can be recovered at a later developmental stage (Yu et al, 2009;Zhou et al, 2009;Chi et al, 2010;Cao et al, 2011;Gong et al, 2014;Hu et al, 2014), the severe albino phenotype of al1 eventually resulted in a lethal phenotype of al1 seedlings at a later developmental stage. Since the level of chlorophyll is one of the most important indicators for Figure 1.…”

“…So far, most of the helical repeat proteins mentioned above were identified from Arabidopsis and green algae. Only a few of them were isolated from rice (Oryza sativa), such as YSA, ECB2-1, and OsV4 (Cao et al, 2011;Su et al, 2012;Gong et al, 2014). To our knowledge, the role of RAP in chloroplast development is still unknown in rice.…”

“…PPR proteins in chloroplast have been implicated as being involved in regulating RNA splicing (Schmitz-Linneweber et al, 2006;de Longevialle et al, 2007;Ichinose et al, 2012), RNA editing (Kotera et al, 2005;Okuda et al, 2007;Chateigner-Boutin et al, 2008;Cai et al, 2009;Yu et al, 2009;Zhou et al, 2009;Tseng et al, 2010;Sosso et al, 2012), RNA cleavage (Meierhoff et al, 2003;Hattori et al, 2007), and translation (Williams and Barkan, 2003;Tavares-Carreón et al, 2008) during plant development. The disruption of tetratricopeptide repeat or PPR proteins generally causes defects in the development of chloroplast, eventually leading to the albino or chlorotic leaf phenotype in plants (Chi et al, 2008(Chi et al, , 2010Cao et al, 2011;Su et al, 2012;Gong et al, 2014).…”

Establishment of the chloroplast genetic system in rice during early leaf development and at low temperatures

“…Recently, several other genes have been isolated from low temperature-conditional, chloroplast-deficient mutants of rice, such as OsV4 ( virescent 4 ), wlp1 ( white leaf and panicles 1 ), and tcd9 ( thermo-sensitive chloroplast development 9 ; Gong et al, 2014; Jiang et al, 2014; Song et al, 2014). The corresponding genes in OsV4 , wlp1 , and tcd9 mutants encode plastidial pentatricopeptide repeat (PPR) protein, plastid ribosomal protein L13, and a subunit of chaperonin 60 (CP60α) required for chloroplast division, respectively.…”

“…The corresponding genes in OsV4 , wlp1 , and tcd9 mutants encode plastidial pentatricopeptide repeat (PPR) protein, plastid ribosomal protein L13, and a subunit of chaperonin 60 (CP60α) required for chloroplast division, respectively. Similarly to NUS1 , V 2 , V 3 , and ST1 , their functions are speculated to be involved in early chloroplast development at low temperatures (Gong et al, 2014; Jiang et al, 2014; Song et al, 2014). It is possible that these factors are involved in a closely related mechanism to chloroplast protein expression and assembly, which is required at low temperatures, but not essential for chloroplast development during early leaf development at higher temperatures.…”