A maize male gametophyte-specific gene encodes ZmLARP6c1, a potential RNA-binding protein required for competitive pollen tube growth

Abstract

Members of the La-Related Protein family (LARPs) contain a conserved La module, which has been associated with RNA-binding activity. Expression of the maize gene GRMZM2G323499/Zm00001d018613, a member of the LARP family, is highly specific to pollen, based on both transcriptomic and proteomic assays. This suggests a pollen-specific RNA regulatory function for the protein, designated ZmLARP6c1 based on sequence similarity to the LARP6 subfamily in Arabidopsis. To test this hypothesis, a Ds-GFP transposable element insertion in the ZmLarp6c1 gene (tdsgR82C05) was obtained from the Dooner/Du mutant collection. Sequencing confirmed that the Ds-GFP insertion is in an exon, and thus likely interferes with ZmLARP6c1 function. Tracking inheritance of the insertion via its endosperm-expressed GFP indicated that the mutation was associated with reduced transmission from a heterozygous plant when crossed as a male (ranging from 0.5% to 26.5% transmission), but not as a female. Furthermore, this transmission defect was significantly alleviated when less pollen was applied to the silk, reducing competition between mutant and wild-type pollen. Pollen grain diameter measurements and nuclei counts showed no significant differences between wild-type and mutant pollen. However, in vitro, mutant pollen tubes were significantly shorter than those from sibling wild-type plants, and also displayed altered germination dynamics. These results are consistent with the idea that ZmLARP6c1 provides an important regulatory function during the highly competitive progamic phase of male gametophyte development following arrival of the pollen grain on the silk. The conditional, competitive nature of the Zmlarp6c1::Ds male sterility phenotype (i.e., reduced ability to produce progeny seed) points toward new possibilities for genetic control of parentage in crop production.

LARP6 proteins in plants

“…Such studies, in particular if conducted with AtLARP6C, should participate in the discovery of novel actors of male reproduction. Since LARP6C function appears conserved in maize [25] , it should widen our understanding of crop reproduction and seed production. reported from [16] .…”

“…To date functional data are available on vascular plant LARP6 proteins, mostly from Arabidopsis and Zea maize [16,21,25] . Arabidopsis contains three LARP6 proteins (one of each type) [16] and maize six, with one 6A, three 6B and two 6C [25] (Figure 2B).…”

“…To date functional data are available on vascular plant LARP6 proteins, mostly from Arabidopsis and Zea maize [16,21,25] . Arabidopsis contains three LARP6 proteins (one of each type) [16] and maize six, with one 6A, three 6B and two 6C [25] (Figure 2B). In Arabidopsis, LARP6 genes show specific expression profiles, with in particular LARP6C exclusively expressed in pollen from the onset of gametogenesis to the end of fertilization process [21,26,27] .…”

“…In maize, ZmLARP6C1, the pollen specific LARP6, is also required during the progamic phase, with loss-of-function mutants showing reduced male transmission that is the consequence of less competitive pollen. Indeed zmlarp6c1-deficient pollens show altered germination dynamics and PT elongation rates [25] . An assessment of the fertilization ability of mutant maize pollens was not conducted, but already the similarities with Arabidopsis phenotypes during the early steps of the progamic phase, suggest that LARP6C molecular and cellular roles could be conserved in maize and more widely in angiosperms (flowering plants).…”