Albino Leaf 2 is involved in the splicing of chloroplast group I and II introns in rice.

Changhong Liu,Haifeng Peng,Zemin Zhang,Jianjun Zhang,Xionghui Chen,Qingjun Xie,Yi Xing,Haitao Zhu,Jianjie Tan

doi:10.1093/jxb/erw296

Abstract

Chloroplasts play an essential role in plant growth and development through manipulating photosynthesis and the production of hormones and metabolites. Although many genes or regulators involved in chloroplast biogenesis and development have been isolated and characterized, identification of novel components is still lacking. We isolated a rice (Oryza sativa) mutant, termed albino leaf 2 (al2), using genetic screening. Phenotypic analysis revealed that the al2 mutation caused obvious albino leaves at the early developmental stage, eventually leading to al2 seedling death. Electron microscopy investigations indicated that the chloroplast structure was disrupted in the al2 mutants at an early developmental stage and subsequently resulted in the breakdown of the entire chloroplast. Molecular cloning illustrated that AL2 encodes a chloroplast group IIA intron splicing facilitator (CRS1) in rice, which was confirmed by a genetic complementation experiment. Moreover, our results demonstrated that AL2 was constitutively expressed in various tissues, including green and non-green tissues. Interestingly, we found that the expression levels of a subset of chloroplast genes that contain group IIA and IIB introns were significantly reduced in the al2 mutant compared to that in the wild type, suggesting that AL2 is a functional CRS1 in rice. Differing from the orthologous CRS1 in maize and Arabidopsis that only regulates splicing of the chloroplast group II intron, our results demonstrated that the AL2 gene is also likely to be involved in the splicing of the chloroplast group I intron. They also showed that disruption of AL2 results in the altered expression of chloroplast-associated genes, including chlorophyll biosynthetic genes, plastid-encoded polymerases and nuclear-encoded chloroplast genes. Taken together, these findings shed new light on the function of nuclear-encoded chloroplast group I and II intron splicing factors in rice.

Highlights

Chloroplasts are essential for plant development and growth, through manipulating the fixation of CO2 and biosynthesis of carbon skeletons and other physiological processes (Sakamoto et al, 2008; Jarvis and Lopez-Juez, 2013).Accumulating evidence has shown the importance of chloroplast biogenesis and development during germination for plant vitality, seed set and growth (Lopez-Juez and Pyke, 2005; Pogson and Albrecht, 2011)
We found that the expression levels of a subset of chloroplast genes that contain group IIA and IIB introns were significantly reduced in the al2 mutant compared to that in the wild type, suggesting that Albino Leaf 2 (AL2) is a functional chloroplast RNA splicing 1 (CRS1) in rice
We describe the function of a nuclear-encoded splicing factor termed Albino Leaf 2 (AL2) that encodes a chloroplast group IIA intron splicing factor CRS1, which is required for chloroplast development in rice

Summary

Introduction

Accumulating evidence has shown the importance of chloroplast biogenesis and development during germination for plant vitality, seed set and growth (Lopez-Juez and Pyke, 2005; Pogson and Albrecht, 2011). It is evident that nucleus-encoded polymerases (NEPs) and plastidencoded polymerases (PEPs) involved in gene transcription, RNA maturation, protein translation and modification have great effect on the biogenesis of chloroplasts (Hedtke et al, 1997; Pogson and Albrecht, 2011; Yu et al, 2014). Recent studies indicated that a large group of nuclear-encoded pentatricopeptide repeats proteins (PPRs) involved in RNA processing, splicing, editing, stability, maturation and translation are critical for chloroplast development (Pogson and Albrecht, 2011). Twenty group II introns and only one group I intron have been identified in the chloroplast genome of Arabidopsis, whereas 17 group II introns and one group I intron have been described in maize and rice (de Longevialle et al, 2010; Bonen and Vogel, 2001)

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