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

Abstract

Summary Low temperature stress hinders plant growth and chloroplast development and can limit the geographic range of cultivars. In rice, japonica cultivars have greater chilling tolerance than indica cultivars, but the molecular mechanism underlying chilling tolerance is unclear. Here, we report an RNA‐binding protein, DUA1, cloned from the indica cultivar Dular, which exhibits a deficiency in chloroplast development at an early stage of development under low‐temperature conditions. DUA1 shares high sequence homology with the pentatricopeptide repeat family and functions in plastid RNA editing under low‐temperature conditions. Our data suggest that DUA1 can bind to the plastid‐encoded rps8‐182 transcript and disruption of DUA1 activity impairs editing. The RNA editing cofactor WSP1, a partner of DUA1, also participates in chloroplast development at low temperature. Western blot analysis indicates that WSP1 enhances DUA1 stability under low temperatures. DUA1 sequence analyses of rice core germplasm revealed that three major haplotypes of DUA1 and one haplotype showed substantial differences in chlorophyll content under low‐temperature conditions. Variation at DUA1 may play an important role in the adaptation of rice to different growing regions.

Effects of Chilling on the Structure, Function and Development of Chloroplasts

“…Various RNA-binding proteins (RBPs), including pentatricopeptide repeat protein (PPR) and ribonucleoproteins (RNPs), are needed for the response to chilling stress to maintain chloroplast development. The loss of RBP genes results in yellow or bleached leaves, and some mutants even exhibit delayed seed germination accompanied by pale primary leaves ( Kusumi et al, 2011 ; Kupsch et al, 2012 ; Gong et al, 2014 ; Song et al, 2014 ; Xu et al, 2014 ; Wang S. et al, 2016 ; Wu et al, 2016 ; Zhang et al, 2016 ; Cui et al, 2018 ). Moreover, the transcription levels of genes associated with chlorophyll biosynthesis, photosynthesis and chloroplast development are altered by chilling ( Gong et al, 2014 ; Wu et al, 2016 ).…”

The OsABCI7 Transporter Interacts with OsHCF222 to Stabilize the Thylakoid Membrane in Rice

“…Many leaf pigmentation mutants are usually associated with chloroplast development in rice (Wang et al, 2016;Lv et al, 2017;Sun et al, 2017;Cui et al, 2019). In this study, we isolated the constitutively expressed…”

“…In chloroplasts, the thylakoid membrane is regularly stacked to increase the membrane area for a higher photosynthetic efficiency, and a well-developed thylakoid membrane system is also closely associated with chloroplast development (Kobayashi et al, 2007). To date, many genes exhibiting crucial regulatory roles in chloroplast development under low temperatures have been identified (Wang et al, 2016;Sun et al, 2017;Cui et al, 2019), while genetic factors affecting the relationship between chloroplast development and intracellular metabolites are largely unknown.…”

The Role of Chloroplast Gene Expression in Plant Responses to Environmental Stress

“…A recent study revealed that that the low-temperature sensitivity of dua1 is caused by defective RNA editing of the plastid ribosome gene rps8 , which is located 182 nt downstream of the translational start site ( rps8 -182). The edited rps8 transcripts generate RPS8 protein with altered amino acid hydrophobicity, suggesting that RNA editing at rps8 -182 improves low-temperature tolerance in rice by moderating the stability of RPS8 protein under low-temperature conditions [ 76 ]. Chloroplast genomes have very slow rates of sequence evolution, averaging ~5-fold slower than nuclear genomes [ 108 , 109 ], suggesting that chloroplast RNA editing evolved to improve low-temperature tolerance by increasing protein stability.…”

“…In addition, RNA editing, particularly C-to-U base conversion, is a widespread phenomenon in chloroplasts across nearly all plant species [ 48 ]. As discussed above, it is clear that RNA editing is important for plant tolerance of low temperature [ 74 , 75 , 76 ], yet the exact editing sites, and how RNA editing at these sites improves plant tolerance to low temperatures, remain to be explored. Finally, translation and splicing of several chloroplast genes trigger plastid-to-nucleus retrograde signaling and ABA signaling [ 73 , 77 , 79 , 80 , 114 ], but it remains unclear how the signals generated from these processes are transferred out of chloroplasts and integrated into these signaling pathways.…”