WHITE PANICLE3, a Novel Nucleus-Encoded Mitochondrial Protein, Is Essential for Proper Development and Maintenance of Chloroplasts and Mitochondria in Rice.

Hongchang Li,Xianfeng Zhao,Yun Wang,Qian Qian,Lihuang Zhu,Dayong Li,Mingsheng Chen,Guobiao Ji,Jichen Xu,Sodmergen Sodmergen,Guozhen Liu,Wenxue Zhai

doi:10.3389/fpls.2018.00762

Abstract

Mitochondria and chloroplasts are interacting organelles that play important roles in plant development. In addition to a small number proteins encoded by their own genomes, the majority of mitochondrial and chloroplast proteins are encoded in the cell nucleus and imported into the organelle. As a consequence, coordination between mitochondria, chloroplasts, and the nucleus is of crucial importance to plant cells. Variegated mutants are chloroplast-defective mutants and are considered to be ideal models for studying the intercommunication between these organelles. Here, we report the isolation of WHITE PANICLE3 (WP3), a nuclear gene involved in variegation, from a naturally occurring white panicle rice mutant. Disrupted expression of WP3 in the mutant leads to severe developmental defects in both chloroplasts and mitochondria, and consequently causes the appearance of white-striped leaves and white panicles in the mutant plants. Further investigation showed that WP3 encodes a protein most likely targeted to mitochondria and is specifically expressed in rice panicles. Interestingly, we demonstrate that the recessive white-panicle phenotype in the wp3 mutant is inherited in a typical Mendelian manner, while the white-striped leaf phenotype in wp3 is maternally inherited. Our data collectively suggest that the nucleus-encoded mitochondrial protein, WP3, plays an essential role in the regulation of chloroplast development in rice panicles by maintaining functional mitochondria. Therefore, the wp3 mutant is an excellent model in which to explore the communication between the nucleus, mitochondria, and chloroplasts in plant cells.

Highlights

In plant cells, chloroplasts and mitochondria are regarded as interdependent organelles due to their complex metabolic connections, such as metabolism, energy status, and reduction/ oxidation status (Raghavendra and Padmasree, 2003; van Lis and Atteia, 2004)
We noticed that the wp3 mutant plants have white-striped leaves, and it is interesting that the white stripes mostly appear on basal tiller leaves (Figure 1B)
We showed that failed expression of WHITE PANICLE3 (WP3) leads to severe developmental defects in both mitochondria and chloroplasts

Summary

Introduction

Chloroplasts and mitochondria are regarded as interdependent organelles due to their complex metabolic connections, such as metabolism, energy status, and reduction/ oxidation (redox) status (Raghavendra and Padmasree, 2003; van Lis and Atteia, 2004). Fine-level coordination between chloroplasts and mitochondria, namely chloroplastmitochondria cross-talk, is essential for the proper functioning and survival of plant cells. Genetic studies in various plant species have demonstrated the existence and importance of chloroplast-mitochondria cross-talk in the development of these organelles. A reduction in the amount of P-protein, one of the subunits of mitochondrial glycine decarboxylase, leads to decreases in both photosynthetic and growth rates (Heineke et al, 2001). Defects in the barley mitochondrial glycine decarboxylase complex result in chloroplast overreduction and over-energization (Sabar et al, 2000). In Chlamydomonas reinhardtii, delivery of chloroplast tRNAs to mitochondria has been demonstrated to be critical for protein synthesis in mitochondria (Bennoun and Delosme, 1999)

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