Rice FLOURY SHRUNKEN ENDOSPERM 5 Encodes a Putative Plant Organelle RNA Recognition Protein that Is Required for cis-Splicing of Mitochondrial nad4 Intron 1

Liang Wang,Wenwei Zhang,Rongbo Chen,Yihua Wang,Hui Dong,Xuan Teng,Yunlu Tian,Shijia Liu,Xiaokang Jiang,Yue Cai,Haigang Yan,Jianmin Wan,Xi Liu

doi:10.1186/s12284-021-00463-2

Liang Wang, Wenwei Zhang + Show 11 more

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https://doi.org/10.1186/s12284-021-00463-2

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Abstract

BackgroundThe sequences of several important mitochondrion-encoded genes involved in respiration in higher plants are interrupted by introns. Many nuclear-encoded factors are involved in splicing these introns, but the mechanisms underlying this splicing remain unknown.ResultsWe isolated and characterized a rice mutant named floury shrunken endosperm 5 (fse5). In addition to having floury shrunken endosperm, the fse5 seeds either failed to germinate or produced seedlings which grew slowly and died ultimately. Fse5 encodes a putative plant organelle RNA recognition (PORR) protein targeted to mitochondria. Mutation of Fse5 hindered the splicing of the first intron of nad4, which encodes an essential subunit of mitochondrial NADH dehydrogenase complex I. The assembly and NADH dehydrogenase activity of complex I were subsequently disrupted by this mutation, and the structure of the mitochondria was abnormal in the fse5 mutant. The FSE5 protein was shown to interact with mitochondrial intron splicing factor 68 (MISF68), which is also a splicing factor for nad4 intron 1 identified previously via yeast two-hybrid (Y2H) assays.ConclusionFse5 which encodes a PORR domain-containing protein, is essential for the splicing of nad4 intron 1, and loss of Fse5 function affects seed development and seedling growth.

Highlights

The sequences of several important mitochondrion-encoded genes involved in respiration in higher plants are interrupted by introns
Other proteins participate in splicing mitochondrial introns, including the following: the DEXH-box-containing RNA helicases AtABO6 and AtPMH2 (Köhler et al 2010; He et al 2012); nuclear-encoded maturases nMAT1 (Nakagawa and Sakurai 2006; Keren et al 2012), nMAT2 (Keren et al 2009), and nMAT4 (Cohen et al 2014); RCC1 family protein RUG3 (Kühn et al 2011); mitochondrial transcription termination factor mTERF15 (Hsu et al 2014); and RAD52-like protein ODB1 (Gualberto et al 2015)
The results showed that the accumulation of complex I in the fse5 mutant was much lower than that in the WT, and NADH dehydrogenase activity was almost completely abolished (Fig. 7a)

Summary

Introduction

The sequences of several important mitochondrion-encoded genes involved in respiration in higher plants are interrupted by introns. Many nuclear-encoded factors are involved in splicing these introns, but the mechanisms underlying this splicing remain unknown. A minor portion of mitochondrial genes are retained in According to their structural features and splicing mechanisms, mitochondrial introns in flowering plants can be divided into group I members and group II members, with the latter being more predominant (Bonen 2008). Group II introns are involved in both cis-splicing and trans-splicing. Various nuclear-encoded proteins are involved in splicing mitochondrial introns in higher plants. Other proteins participate in splicing mitochondrial introns, including the following: the DEXH-box-containing RNA helicases AtABO6 and AtPMH2 (Köhler et al 2010; He et al 2012); nuclear-encoded maturases nMAT1 (Nakagawa and Sakurai 2006; Keren et al 2012), nMAT2 (Keren et al 2009), and nMAT4 (Cohen et al 2014); RCC1 family protein RUG3 (Kühn et al 2011); mitochondrial transcription termination factor mTERF15 (Hsu et al 2014); and RAD52-like protein ODB1 (Gualberto et al 2015)

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