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ZmCTLP1 is required for the maintenance of lipid homeostasis and the basal endosperm transfer layer in maize kernels.

ABSTRACT: Maize kernel weight is influenced by the unloading of nutrients from the maternal placenta and their passage through the transfer tissue of the basal endosperm transfer layer (BETL) and the basal intermediate zone (BIZ) to the upper part of the endosperm. Here, we show that Small kernel 10 (Smk10) encodes a choline transporter-like protein 1 (ZmCTLP1) that facilitates choline uptake and is located in the trans-Golgi network (TGN). Its loss of function results in reduced choline content, leading to smaller kernels with a lower starch content. Mutation of ZmCTLP1 disrupts membrane lipid homeostasis and the normal development of wall in-growths. Expression levels of Mn1 and ZmSWEET4c, two kernel filling-related genes, are downregulated in the smk10, which is likely to be one of the major causes of incompletely differentiated transfer cells. Mutation of ZmCTLP1 also reduces the number of plasmodesmata (PD) in transfer cells, indicating that the smk10 mutant is impaired in PD formation. Intriguingly, we also observed premature cell death in the BETL and BIZ of the smk10 mutant. Together, our results suggest that ZmCTLP1-mediated choline transport affects kernel development, highlighting its important role in lipid homeostasis, wall in-growth formation and PD development in transfer cells.

SUBMITTER: Hu M

PROVIDER: S-EPMC9292782 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: In plant, non-specific lipid transfer proteins (nsLTPs) are small, basic proteins that have been reported to be involved in numerous biological processes such as transfer of phospholipids, reproductive development, pathogen defence and abiotic stress response. To date, only a tiny fraction of plant nsLTPs have been functionally identified, and even fewer have been identified in maize [Zea mays (Zm)]. RESULTS: In this study, we carried out a genome-wide analysis of nsLTP gene family in maize and identified 63 nsLTP genes, which can be divided into five types (1, 2, C, D and G). Similar intron/exon structural patterns were observed in the same type, strongly supporting their close evolutionary relationship. Gene duplication analysis indicated that both tandem and segmental duplication contribute to the diversification of this gene family. Additionally, the three-dimensional structures of representative nsLTPs were studied with homology modeling to understand their molecular functions. Gene ontology analysis was performed to obtain clues about biological function of the maize nsLTPs (ZmLTPs). The analyses of putative upstream regulatory elements showed both shared and distinct transcriptional regulation motifs of ZmLTPs, further indicating that ZmLTPs may play roles in diverse biological processes. The dynamic expression patterns of ZmLTPs family across the different developmental stages showed that several of them exhibit tissue-specific expression, indicative of their important roles in maize life cycle. Furthermore, we focused on the roles of maize nsLTPs in biotic and abiotic stress responses. Our analyses demonstrated that some ZmLTPs exhibited a delayed expression pattern after the infection of Ustilago maydis and differentially expressed under drought, salt and cold stresses, and these may be a great help for further studies to improve the stress resistance and tolerance in maize breeding. CONCLUSIONS: Our results provide new insights into the phylogenetic relationships and characteristic functions of maize nsLTPs and will be useful in studies aimed at revealing the global regulatory network in maize development and stress responses, thereby contributing to the maize molecular breeding with enhanced quality traits.

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ZmCTLP1 is required for the maintenance of lipid homeostasis and the basal endosperm transfer layer in maize kernels.

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