The evolution of RNA helicases and their roles for plant sexual and apomictic reproduction
Plant Cell and Developmental Biology
Final Report Abstract
In higher plants sexual and asexual reproduction (apomixis) are alternative strategies for seed formation. Apomixis has long been recognized for its great potential for applications in agriculture, as it leads to the formation of clonal offspring. A precondition for engineering of apomixis in crop species would be a precise understanding of the genetic and gene regulatory basis underlying. To gain detailed insights into the transcriptional basis governing the development of the female germline in apomicts, we used the genus Boechera for tissue type-specific analysis, which is a close relative of Arabidopsis. This uncovered the differential activity of F-box genes and E3 ligases upon germline formation in sexual as compared to apomictic accessions and confirmed abundant expression of RNA helicases. At late stages of germline development in tissues harboring mature gametophytes, a small number of RNA helicases were consistently differentially expressed between samples from either reproductive mode. This designates them as potential candidates for determining aspects of cell-type specification. Interestingly, in partial contradiction to the classical hypothesis of an accumulation of deleterious mutations due to asexual reproduction, based on allelic variants identified by targeted sequencing from 24 sexual or apomictic Boechera accessions, the coding sequences of 58 RNA helicases investigated are largely conserved and under purifying selection also in apomicts. This suggests that deleterious mutations in genes with fundamental roles in cellular or developmental processes typically do not reach fixation independent of the reproductive mode. In line with this, we already could confirm the crucial importance of some of the RNA helicases for reproduction. Importantly, we demonstrated that Arabidopsis RH17 is involved in restricting germline fate and in repressing aspects of autonomous seed development in the absence of fertilization. Based on spatial and temporal expression in sexual and apomictic Boechera, an additional RNA helicase was identified as candidate for controlling aspects of gametogenesis. Consistently, lines carrying mutant alleles of this gene show male and female gametophytic lethality. Moreover, unlike the Arabidopsis gene which is represented by a single copy, in Boechera one ortholog and two paralogs are found. Current investigations focus on the investigation of their putative functional diversification. Taken together, the study provided important new insights into the gene regulatory basis of plant reproduction involving RNA helicases and a very good basis for future studies on their precise molecular roles.
Publications
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(2019) Differential activity of F-box genes and E3 ligases distinguishes sexual versus apomictic germline specification in Boechera. J. Exp. Bot. 70(20):5643-5657
Zühl L, Volkert C, Ibberson D, Schmidt A
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(2020) Controlling apomixis: Shared features and distinct characteristics of gene regulation. Genes 11(3):329
Schmidt A
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(2020) Gene function rather than reproductive mode drives the evolution of RNA helicases in sexual and apomictic Boechera. Genome Biol Evol. 12(5):656-673
Kiefer M, Nauerth BH, Volkert C, Ibberson D, Loreth A, Schmidt A
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(2021). RH17 acts in repression of reproductive fate and autonomous seed coat development in Arabidopsis. Development. 148, dev198739
Stein RE, Nauerth BH, Binmöller L, Zühl L, Loreth A, Reinert M, Ibberson D, Schmidt A
