biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 68:152-160, 2024 | DOI: 10.32615/bp.2024.014

OsPPR19, a rice pentatricopeptide repeat protein, is essential for mitochondrial biogenesis and seed development

Kwanuk LEE1, *, Su Jung PARK2, Yeon-Ok KIM2, Jong-Seong JEON3, Hunseung KANG2, *
1 Department of Biology, Jeju National University, Jeju 63243, Korea
2 Department of Applied Biology, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, Korea
3 Graduate School of Green-Bio Science and Crop Biotech Institute, Kyung Hee University, Yongin 17104, Korea

Despite the accumulating evidence showing the essential role of pentatricopeptide repeat (PPR) proteins in organellar biogenesis and plant development in Arabidopsis thaliana and maize (Zea mays), the functions of most PPR proteins in rice (Oryza sativa) are still unknown. A former study demonstrated that the mitochondria-localized Arabidopsis PPR19 is crucial for mitochondrial function and normal plant growth and development. In this study, we characterized the functional role of a rice ortholog (LOC_Os12g04110) of Arabidopsis PPR19 protein. The loss-of-function osppr19 mutant displayed delayed seed germination and stunted root and seedling growth compared with wild-type. The height of the osppr19 mutant was significantly shorter, and the grain mass of the mutant was lower than that of the wild-type. The osppr19 mutant carried few filled grains and a higher number of aborted seeds than the wild-type. The structures of mitochondria in the osppr19 mutant were abnormal, and more reactive oxygen species were accumulated in the mutant, suggesting defective mitochondrial biogenesis and function in the osppr19 mutant. Importantly, the amount of mature mitochondrial transcripts was significantly decreased in the mutant. Taken together, these results suggest that the mitochondrial OsPPR19 is essential for mitochondrial biogenesis and function, which is crucial for plant growth and development of rice grain.

Keywords: intron splicing, mitochondria, pentatricopeptide repeat, rice, seed development.

Received: March 26, 2024; Revised: September 2, 2024; Accepted: September 24, 2024; Published online: October 8, 2024  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
LEE, K., Jung PARK, S., Yeon-Ok, K., JEON, J., & KANG, H. (2024). OsPPR19, a rice pentatricopeptide repeat protein, is essential for mitochondrial biogenesis and seed development. Biologia plantarum, 68, Article 152-160. https://doi.org/10.32615/bp.2024.014
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download file7146_Lee_Suppl.pdf

    File size: 696.38 kB

    References

    1. Alexander, M.P. (1969) Differential staining of aborted and nonaborted pollen. Stain Technology, 44, 117-122. Go to original source...
    2. Andersson, S.G.E., Karlberg, O., Canbäck, B. & Kurland, C.G. (2003) On the origin of mitochondria: a genomics perspective. Philosophical Transactions of the Royal Society B, 358, 165-177. Go to original source...
    3. Barkan, A. & Small, I. (2014) Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology, 65, 415-442. Go to original source...
    4. Bentolila, S., Alfonso, A.A. & Hanson, M.R. (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proceedings of the National Academy of Sciences, 99, 10887-10892. Go to original source...
    5. Best, C., Mizrahi, R., Edris, R. et al. (2023) MSP1 encodes an essential RNA-binding pentatricopeptide repeat factor required for nad1 maturation and complex I biogenesis in Arabidopsis mitochondria. New Phytologist, 238, 2375-2392. Go to original source...
    6. Brown, G.G., Formanová, N., Jin, H. et al. (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. The Plant Journal, 35, 262-272. Go to original source...
    7. Budar, F., Touzet, P. & De Paepe, R. (2003) The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica, 117, 3-16. Go to original source...
    8. Cai, M., Li, S., Sun, F. et al. (2017) Emp10 encodes a mitochondrial PPR protein that affects the cis-splicing of nad2 intron 1 and seed development in maize. The Plant Journal, 91, 132-144. Go to original source...
    9. Chen, X., Feng, F., Qi, W. et al. (2017) Dek35 encodes a PPR protein that affects cis-splicing of mitochondrial nad4 intron 1 and seed development in maize. Molecular Plant, 10, 427-441. Go to original source...
    10. Cheng, S., Gutmann, B., Zhong, X. et al. (2016) Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. The Plant Journal, 85, 532-547. Go to original source...
    11. Colas des Francs-Small, C., Falcon de Longevialle, A., Li, Y.H. et al. (2014) The pentatricopeptide repeat proteins TANG2 and ORGANELLE TRANSCRIPT PROCESSING439 are involved in the splicing of the multipartite nad5 transcript encoding a subunit of mitochondrial complex I. Plant Physiology, 165, 1409-1416. Go to original source...
    12. Dinh, S.N., Park, S.J., Han, J.H. & Kang, H. (2019) A chloroplast-targeted S1 RNA-binding domain protein plays a role in Arabidopsis response to diverse abiotic stresses. Journal of Plant Biology, 62, 74-81. Go to original source...
    13. Falcon de Longevialle, A., Meyer, E.H., Andrés, C. et al. (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. The Plant Cell, 19, 3256-3265. Go to original source...
    14. Fan, K., Ren, Z., Zhang, X. et al. (2021) The pentatricopeptide repeat protein EMP603 is required for the splicing of mitochondrial nad1 intron 2 and seed development in maize. Journal of Experimental Botany, 72, 6933-6948. Go to original source...
    15. Hammani, K. & Giegé, P. (2014) RNA metabolism in plant mitochondria. Trends in Plant Science, 19, 380-389. Go to original source...
    16. Hsieh, W.-Y., Liao, J.-C., Chang, C.-Y., Harrison, T., Boucher. C. & Hsieh, M.-H. (2015) The SLOW GROWTH3 pentatricopeptide repeat protein is required for the splicing of mitochondrial NADH dehydrogenase subunit7 intron 2 in Arabidopsis. Plant Physiology, 168, 490-501. Go to original source...
    17. Hu, J., Huang, W., Huang, Q. et al. (2014) Mitochondria and cytoplasmic male sterility in plants. Mitochondrion, 19, 282-288. Go to original source...
    18. Hu, J., Wang, K., Huang, W. et al. (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. The Plant Cell, 24, 109-122. Go to original source...
    19. Jeon, J.-S., Lee, S., Jung, K.-H. et al. (2000) T-DNA insertional mutagenesis for functional genomics in rice. The Plant Journal, 22, 561-570. Go to original source...
    20. Jeong, D.H., An, S., Park, S. et al. (2006) Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. The Plant Journal, 45, 123-132. Go to original source...
    21. Jung, L., Schleicher, S., Taha, F.A., Takenaka, M. & Binder, S. (2023) The MITOCHONDRIAL TRANSCRIPT STABILITY FACTOR 4 (MTSF4) is essential for the accumulation of dicistronic rpl5-cob mRNAs in Arabidopsis thaliana. The Plant Journal, 113, 375-386. Go to original source...
    22. Kim, J., Nguyen, T.-N.L. & Kang, H. (2017) Artificial targeting of a nucleus-encoded RNA-binding protein AtRZ1a to chloroplasts affects flowering and ABA response of Arabidopsis thaliana. Journal of Plant Biology, 60, 278-284. Go to original source...
    23. Koizuka, N., Imai, R., Fujimoto, H. et al. (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. The Plant Journal, 34, 407-415. Go to original source...
    24. Koprivova, A., Colas des Francs-Small, C., Calder, G. et al. (2010) Identification of a pentatricopeptide repeat protein implicated in splicing of intron 1 of mitochondrial nad7 transcripts. Journal of Biological Chemistry, 285, 32192-32199. Go to original source...
    25. Lee, K. (2023) Relocation of chloroplast proteins from cytosols into chloroplasts. Plant Signaling and Behavior, 18, 2258321. Go to original source...
    26. Lee, K., Han, J.H., Park, Y.-I., Colas des Francs-Small, C., Small, I. & Kang H. (2017) The mitochondrial pentatricopeptide repeat protein PPR19 is involved in the stabilization of NADH dehydrogenase 1 transcripts and is crucial for mitochondrial function and Arabidopsis thaliana development. New Phytologist, 215, 202-216. Go to original source...
    27. Lee, K., Park, S.J., Colas des Francs-Small, C., Whitby, M., Small, I. & Kang H. (2019) The coordinated action of PPR4 and EMB2654 on each intron half mediates trans-splicing of rps12 transcripts in plant chloroplasts. The Plant Journal, 100, 1193-1207. Go to original source...
    28. Liu, R., Cao, S.-K., Sayyed, A. et al. (2020) The mitochondrial pentatricopeptide repeat protein PPR18 is required for the cis-splicing of nad4 intron 1 and essential to seed development in maize. International Journal of Molecular Sciences, 21, 4047. Go to original source...
    29. Liu, Y., He, J.N., Chen, Z.Z., Ren, X.Z., Hong, X.H. & Gong Z.Z. (2010) ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis. The Plant Journal, 63, 749-765. Go to original source...
    30. Lurin, C., Andreés, C., Aubourg, S. et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. The Plant Cell, 16, 2089-2103. Go to original source...
    31. Millar, A.H., Heazlewood, J.L., Kristensen, B.K., Braun, H.-P. & Møller, I.M. (2005) The plant mitochondrial proteome. Trends in Plant Science, 10, 36-43. Go to original source...
    32. Millar, A.H., Whelan, J. & Small, I. (2006) Recent surprises in protein targeting to mitochondria and plastids. Current Opinion in Plant Biology, 9, 610-615. Go to original source...
    33. Pan, Z., Liu, M., Xiao, Z. et al. (2019) ZmSMK9, a pentatricopeptide repeat protein, is involved in the cis-splicing of nad5, kernel development and plant architecture in maize. Plant Science, 288, 110205. Go to original source...
    34. Qiu, T., Zhao, X., Feng, H. et al. (2021) OsNBL3, a mitochondrion-localized pentatricopeptide repeat protein, is involved in splicing nad5 intron 4 and its disruption causes lesion mimic phenotype with enhanced resistance to biotic and abiotic stresses. Plant Biotechnology Journal, 19, 2277-2290. Go to original source...
    35. Ramel, F., Sulmon, C., Bogard, M., Couée, I. & Gouesbet, G. (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biology, 9, 28. Go to original source...
    36. Ren, X., Pan, Z., Zhao, H. et al. (2017) EMPTY PERICARP11 serves as a factor for splicing of mitochondrial nad1 intron and is required to ensure proper seed development in maize. Journal of Experimental Botany, 68, 4571-4581. Go to original source...
    37. Schmitz-Linneweber, C. & Small, I. (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends in Plant Science, 13, 663-670. Go to original source...
    38. Sun, F., Xiu, Z., Jiang, R. et al. (2019) The mitochondrial pentatricopeptide repeat protein EMP12 is involved in the splicing of three nad2 introns and seed development in maize. Journal of Experimental Botany, 70, 963-972. Go to original source...
    39. Wang, C., Aubé, F., Planchard, N. et al. (2017) The pentatrico­peptide repeat protein MTSF2 stabilizes a nad1 precursor transcript and defines the 3' end of its 5'-half intron. Nucleic Acids Research, 45, 6119-6134. Go to original source...
    40. Wang, Z., Zou, Y., Li, X. et al. (2006) Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. The Plant Cell, 18, 676-687. Go to original source...
    41. Wu, M., Ren, Y., Cai, M. et al. (2019) Rice FLOURY ENDOSPERM 10 encodes a pentatricopeptide repeat protein that is essential for the trans-splicing of mitochondrial nad1 intron 1 and endosperm development. New Phytologist, 223, 736-750. Go to original source...
    42. Xiu, Z., Sun, F., Shen, Y. et al. (2016) EMPTY PERICARP16 is required for mitochondrial nad2 intron 4 cis-splicing, complex I assembly and seed development in maize. The Plant Journal, 85, 507-519. Go to original source...
    43. Yang, Y.-Z., Ding, S., Liu, X.-Y. et al. (2021) EMP32 is required for the cis-splicing of nad7 intron 2 and seed development in maize. RNA Biology, 18, 499-509. Go to original source...
    44. Zhang, L., Chen, J., Zhang, L. et al. (2021) The pentatricopeptide repeat protein EMB1270 interacts with CFM2 to splice specific group II introns in Arabidopsis chloroplasts. Journal of Integrative Plant Biology, 63, 1952-1966. Go to original source...
    45. Zhang, Q., Chen, C., Wang, Y. et al. (2023) OsPPR11 encoding P-type PPR protein that affects group II intron splicing and chloroplast development. Plant Cell Reports, 42, 421-431. Go to original source...
    46. Zhao, P., Wang, F., Li, N., Shi, D.-Q. & Yang, W.-C. (2020) Pentatricopeptide repeat protein MID1 modulates nad2 intron 1 splicing and Arabidopsis development. Scientific Reports, 10, 2008. Go to original source...
    47. Zheng, P., Liu, Y., Liu, X. et al. (2021) OsPPR939, a nad5 splicing factor, is essential for plant growth and pollen development in rice. Theoretical and Applied Genetics, 134, 923-940. Go to original source...

    Return to the content