Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in Maize

Mitochondrial genes in flowering plants contain predominantly group II introns that require precise splicing before translation into functional proteins. Splicing of these introns is facilitated by various nucleus-encoded splicing factors. Due to lethality of mutants, functions of many splicing fact...

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Main Authors: Huanhuan Yang, Zhihui Xiu, Le Wang, Shi-Kai Cao, Xiulan Li, Feng Sun, Bao-Cai Tan
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.00732/full
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spelling doaj-f69a63fbfcd54858b94a4487d9a532f22020-11-25T02:26:58ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-06-011110.3389/fpls.2020.00732534652Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in MaizeHuanhuan YangZhihui XiuLe WangShi-Kai CaoXiulan LiFeng SunBao-Cai TanMitochondrial genes in flowering plants contain predominantly group II introns that require precise splicing before translation into functional proteins. Splicing of these introns is facilitated by various nucleus-encoded splicing factors. Due to lethality of mutants, functions of many splicing factors have not been revealed. Here, we report the function of two P-type PPR proteins PPR101 and PPR231, and their role in maize seed development. PPR101 and PPR231 are targeted to mitochondria. Null mutation of PPR101 and PPR231 arrests embryo and endosperm development, generating empty pericarp and small kernel phenotype, respectively, in maize. Loss-of-function in PPR101 abolishes the splicing of nad5 intron 2, and reduces the splicing of nad5 intron 1. Loss-of-function in PPR231 reduces the splicing of nad5 introns 1, 2, 3 and nad2 intron 3. The absence of Nad5 protein eliminates assembly of complex I, and activates the expression of alternative oxidase AOX2. These results indicate that both PPR101 and PPR231 are required for mitochondrial nad5 introns 1 and 2 splicing, while PPR231 is also required for nad5 intron 3 and nad2 intron 3. Both genes are essential to complex I assembly, mitochondrial function, and maize seed development. This work reveals that the splicing of a single intron involves multiple PPRs.https://www.frontiersin.org/article/10.3389/fpls.2020.00732/fullPPR proteinsgroup II intron splicingnad5complex I biogenesismitochondriamaize seed development
collection DOAJ
language English
format Article
sources DOAJ
author Huanhuan Yang
Zhihui Xiu
Le Wang
Shi-Kai Cao
Xiulan Li
Feng Sun
Bao-Cai Tan
spellingShingle Huanhuan Yang
Zhihui Xiu
Le Wang
Shi-Kai Cao
Xiulan Li
Feng Sun
Bao-Cai Tan
Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in Maize
Frontiers in Plant Science
PPR proteins
group II intron splicing
nad5
complex I biogenesis
mitochondria
maize seed development
author_facet Huanhuan Yang
Zhihui Xiu
Le Wang
Shi-Kai Cao
Xiulan Li
Feng Sun
Bao-Cai Tan
author_sort Huanhuan Yang
title Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in Maize
title_short Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in Maize
title_full Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in Maize
title_fullStr Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in Maize
title_full_unstemmed Two Pentatricopeptide Repeat Proteins Are Required for the Splicing of nad5 Introns in Maize
title_sort two pentatricopeptide repeat proteins are required for the splicing of nad5 introns in maize
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2020-06-01
description Mitochondrial genes in flowering plants contain predominantly group II introns that require precise splicing before translation into functional proteins. Splicing of these introns is facilitated by various nucleus-encoded splicing factors. Due to lethality of mutants, functions of many splicing factors have not been revealed. Here, we report the function of two P-type PPR proteins PPR101 and PPR231, and their role in maize seed development. PPR101 and PPR231 are targeted to mitochondria. Null mutation of PPR101 and PPR231 arrests embryo and endosperm development, generating empty pericarp and small kernel phenotype, respectively, in maize. Loss-of-function in PPR101 abolishes the splicing of nad5 intron 2, and reduces the splicing of nad5 intron 1. Loss-of-function in PPR231 reduces the splicing of nad5 introns 1, 2, 3 and nad2 intron 3. The absence of Nad5 protein eliminates assembly of complex I, and activates the expression of alternative oxidase AOX2. These results indicate that both PPR101 and PPR231 are required for mitochondrial nad5 introns 1 and 2 splicing, while PPR231 is also required for nad5 intron 3 and nad2 intron 3. Both genes are essential to complex I assembly, mitochondrial function, and maize seed development. This work reveals that the splicing of a single intron involves multiple PPRs.
topic PPR proteins
group II intron splicing
nad5
complex I biogenesis
mitochondria
maize seed development
url https://www.frontiersin.org/article/10.3389/fpls.2020.00732/full
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