Fitness effects of somatic mutations accumulating during vegetative growth

Abstract

The unique life form of plants promotes the accumulation of somatic mutations that can be passed to offspring in the next generation, because the same meristem cells responsible for vegetative growth also generate gametes for sexual reproduction. However, little is known about the consequences of somatic mutation accumulation for offspring fitness. We evaluate the fitness effects of somatic mutations in Mimulus guttatus by comparing progeny from self-pollinations made within the same flower (autogamy) to progeny from self-pollinations made between stems on the same plant (geitonogamy). The effects of somatic mutations are evident from this comparison, as autogamy leads to homozygosity of a proportion of somatic mutations, but progeny from geitonogamy remain heterozygous for mutations unique to each stem. In two different experiments, we find consistent fitness effects of somatic mutations from individual stems. Surprisingly, several progeny groups from autogamous crosses displayed increases in fitness compared to progeny from geitonogamy crosses, likely indicating that beneficial somatic mutations occurred in some stems. These results support the hypothesis that somatic mutations accumulate during vegetative growth, but they are filtered by different forms of selection that occur throughout development, resulting in the culling of expressed deleterious mutations and the retention of beneficial mutations.

Are mutations usually deleterious? A perspective on the fitness effects of mutation accumulation

“…In most MA studies on animals, only a single individual or pair is allowed to contribute to the next generation, ensuring that N e is small. In plants, single seeds can be used to propagate each MA line, but because plants do not have a segregated set of germlines cells, they are subject to clonal selection in the meristem Klekowski and Kazarinova-Fukshansky 1984;Otto and Orive 1995;Otto and Hastings 1998;Schoen and Schultz 2019;Cruzan et al 2022), which may prevent some harmful mutations from being passed to the next generation. Similarly, more gene expression takes place in the male gametes of plants relative to animals, potentially exposing recessive mutations to selection (Mulachy et al 1996;Otto et al 2015).…”

Epigenomics as Potential Tools for Enhancing Magnitude of Breeding Approaches for Developing Climate Resilient Chickpea

“…Epigenetic modification has the ability to memorize the event over a long time as a plant molecular memory and the ability to respond rapidly with heritable phenotypic characteristics as an inheritance system against environmental fluxes. Some extreme abiotic stress treatments can lead to plant genome reorganization (Klumpp et al, 2004;Molinier et al, 2006) but few reports are indicating that short-term stress causes a large number of genomic mutations (Lämke and Bäurle, 2017;Cruzan et al, 2018). More evidence supports the speculation that plant stress memory is mainly regulated by epigenetic pathways (Tang et al, 2014), which means changing the expression pattern of the entire genome to form a rebalanced genome expression system, without changing the genome sequence (Habu et al, 2001;Madlung and Comai, 2004).…”

Genetic diversity within a tree and alternative indexes for different evolutionary effects

“…Empirical studies on the accumulation of somatic mutations of trees and clonal plants yielded varying conclusions:Ally et al (2010) reported a decline in fertility,Bobiwash et al (2013) estimated the accumulation of deleterious mutations in a long-lived clonal shrub. In contrast,Cruzan et al (2022) found within-individual selection in perennial herbs resulting in the production of advantageous mutations in some shoots, whileAlejano et al (2019) observed no correlation between fitness of offspring and the age of the parent tree. More empirical studies are needed.…”