The DEAD‐box RNA helicase ZmRH48 is required for the splicing of multiple mitochondrial introns, mitochondrial complex biosynthesis, and seed development in maize

• Published in: Journal of integrative plant biology Vol. 65; no. 11; pp. 2456 - 2468
• Main Authors: Yang, Yan‐Zhuo, Ding, Shuo, Liu, Xin‐Yuan, Xu, Chunhui, Sun, Feng, Tan, Bao‐Cai
• Format: Journal Article
• Language: English
• Published: Hoboken Wiley Subscription Services, Inc 01.11.2023; Key Laboratory of Plant Development and Environmental Adaptation Biology,Ministry of Education,School of Life Sciences,Shandong University,Qingdao 266237,China
• Subjects: Adenosine triphosphate; ATP; Biosynthesis; Corn; DNA helicase; Embryogenesis; Embryonic growth stage; Endosperm; intron splicing; Introns; maize; Metabolism; Mitochondria; Plant physiology; Protein turnover; Proteins; RNA helicase; seed development; Seeds; Splicing; Zea mays; ZmRH48; seed development; intron splicing; maize; mitochondria; ZmRH48; RNA helicase
• ISSN: 1672-9072; 1744-7909
• DOI: 10.1111/jipb.13558

ABSTRACT RNA helicases participate in nearly all aspects of RNA metabolism by rearranging RNAs or RNA–protein complexes in an adenosine triphosphate‐dependent manner. Due to the large RNA helicase families in plants, the precise roles of many RNA helicases in plant physiology and development remain to be clarified. Here, we show that mutations in maize (Zea mays) DEAD‐box RNA helicase 48 (ZmRH48) impair the splicing of mitochondrial introns, mitochondrial complex biosynthesis, and seed development. Loss of ZmRH48 function severely arrested embryogenesis and endosperm development, leading to defective kernel formation. ZmRH48 is targeted to mitochondria, where its deficiency dramatically reduced the splicing efficiency of five cis‐introns (nad5 intron 1; nad7 introns 1, 2, and 3; and ccmFc intron 1) and one trans‐intron (nad2 intron 2), leading to lower levels of mitochondrial complexes I and III. ZmRH48 interacts with two unique pentatricopeptide repeat (PPR) proteins, PPR‐SMR1 and SPR2, which are required for the splicing of over half of all mitochondrial introns. PPR‐SMR1 interacts with SPR2, and both proteins interact with P‐type PPR proteins and Zm‐mCSF1 to facilitate intron splicing. These results suggest that ZmRH48 is likely a component of a splicing complex and is critical for mitochondrial complex biosynthesis and seed development. The molecular mechanism underlying intron splicing in plant organelles remains largely unclear. Here, we found that the DEAD‐box RNA helicase ZmRH48 plays an important role in intron splicing by interacting with two unique PPR proteins, PPR‐SMR1 and SPR2, in maize mitochondria. They are likely components of a splicing complex.