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White and green striate leaves 1, predicted to encode a 16S rRNA processing protein, plays a critical role in the processing of chloroplast ribosomes in maize (Zea mays L.)

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Abstract

Ribosomes play a crucial role in protein biosynthesis and are linked to plant growth and development. The RimM protein has been shown to be involved in the maturation of 30S ribosomal subunits, but its exact function in plants is still unknown. In this study, we discovered a maize mutant with white and green striate leaves (wgsl1) and reduced chlorophyll content. Genetic analysis showed that the wgsl1 mutation was recessive and controlled by a single nuclear gene. Map-based cloning of ZmWGSL1 identified a base substitution (G to A) that generated a missense mutation within the Zm00001d039036 gene in the wgsl1 mutant. Zm00001d039036 encodes a 16S rRNA processing protein containing the RimM motif. Further analysis of transcriptomic data showed that the transcript levels of many ribosomal proteins involved in the small and big ribosomal subunits were dramatically up-regulated in the wgsl1 mutant. Moreover, the level of ribosomal multimers was decreased. This suggests that ZmWGSL1 plays a crucial role in the maturation of the ribosome, leading to abnormal plant growth and development. In addition, subcellular localization results indicate that WGSL1 is localized in chloroplasts. Therefore, we suggest that WGSL1 is a nuclear-encoded protein, is transported to the chloroplast to drive functions, and affects the processing of ribosomes in the chloroplast.

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Data availability

The RNA datasets reported in this study have been deposited in GenBank (NCBI) with under accession number: PRJNA940905.

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Acknowledgements

This study was funded by the National Natural Science Foundation of China (31771803 and 31771802), the Taishan Scholars Program of Shandong Province (tsqn201909074), the Key Projects of the Natural Science Foundation of Shandong Province (ZR2020KC019), and the Natural Science Foundation of Shandong Province (ZR2022MC076).

Funding

This study was supported by the National Natural Science Foundation of China, Grant/Award Number: 31771803 and 31771802; the Taishan Scholars Program of Shandong Province, Grant/Award Number: tsqn201909074; the Key Projects of the Natural Science Foundation of Shandong Province, Grant/Award Number: ZR2020KC019; and the Natural Science Foundation of Shandong Province, Grant/Award Number: ZR2022MC076.

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Q.L., D.J., G.P., Z.Z, G.L., and H.D. designed and carried out the experiment, analyzed the data, and wrote the manuscript. Q.L., D.J., Z.Q., C.P., W.H., L.Z., X.L., Y.N., and X.L. contributed to plant materials management, phenotypic evaluation and fine mapping of wgsl1. G.L. and H.D. critically read the manuscript.

Corresponding authors

Correspondence to Gaoke Li or Haiping Ding.

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Supplementary materials

ESM 1

The following are available online at www.mdpi.com/xxx/s1: Supplementary Figure 1, the white-green stripe phenotype of wgsl1 in early development; Supplementary Figure 2, determination of chlorophyll precursor substance content; Supplementary Figure 3, the photosynthetic rate of the mutant wgsl1 and the WT; Supplementary Figure 4, plant phenotype, ear phenotype, and agronomic traits; Supplementary Figure 5, gene ontology (GO) categories and pathway enrichment of differentially expressed genes between wgsl1 and WT RP125; Supplementary Figure 6, the random selection of RNA sequence data of related pathway genes in Figure 7 was used for quantitative verification; Supplementary Figure 7, phenotypes of T0 generation knockout strains; Supplementary Table 1, population segregation of mutant wgsl1; Supplementary Table 2, preliminary screening of linkage markers for the mutant gene; Supplementary Table 3, fine mapping molecular markers; Supplementary Table 4, primer list of WGSL1 gene amplification and RT- qPCR primers. Supplemental table 5. Primers for knockout strain identification; Supplementary Table 6, transcriptome data validation of RT-qPCR primers. (DOCX 2740 kb)

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Li, Q., Du, J., Qiao, Z. et al. White and green striate leaves 1, predicted to encode a 16S rRNA processing protein, plays a critical role in the processing of chloroplast ribosomes in maize (Zea mays L.). Mol Breeding 43, 65 (2023). https://doi.org/10.1007/s11032-023-01407-y

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