Predictable and stable epimutations induced during clonal plant propagation with embryonic transcription factor

Wibowo, Anjar Tri; Antunez-Sanchez, Javier; Dawson, Alexander; Price, Jonathan; Meehan, Cathal; Wrightsman, Travis; Collenberg, Maximillian; Bezrukov, Ilja; Becker, Claude; Benhamed, Moussa; Weigel, Detlef und Gutierrez-Marcos, Jose (2022): Predictable and stable epimutations induced during clonal plant propagation with embryonic transcription factor.
In: PLOS Genetics 18(11), e1010479

Abstract

Clonal propagation is frequently used in commercial plant breeding and biotechnology programs because it minimizes genetic variation, yet it is not uncommon to observe clonal plants with stable phenotypic changes, a phenomenon known as somaclonal variation. Several studies have linked epigenetic modifications induced during regeneration with this newly acquired phenotypic variation. However, the factors that determine the extent of somaclonal variation and the molecular changes underpinning this process remain poorly understood. To address this gap in our knowledge, we compared clonally propagated Arabidopsis thaliana plants derived from somatic embryogenesis using two different embryonic transcription factors- RWP-RK DOMAIN-CONTAINING 4 (RKD4) or LEAFY COTYLEDON2 (LEC2) and from two epigenetically distinct founder tissues. We found that both the epi(genetic) status of the explant and the regeneration protocol employed play critical roles in shaping the molecular and phenotypic landscape of clonal plants. Phenotypic variation in regenerated plants can be largely explained by the inheritance of tissue-specific DNA methylation imprints, which are associated with specific transcriptional and metabolic changes in sexual progeny of clonal plants. For instance, regenerants were particularly affected by the inheritance of root-specific epigenetic imprints, which were associated with an increased accumulation of salicylic acid in leaves and accelerated plant senescence. Collectively, our data reveal specific pathways underpinning the phenotypic and molecular variation that arise and accumulate in clonal plant populations. Author summary Clonal propagation is commonly used in plants to propagate selected genotypes and to aid genetic/genomic manipulation. Although cloning minimizes genetic variation, clonal plants commonly display phenotypic changes, a phenomenon known as somaclonal variation, that are at times stable after multiple cycles of sexual reproduction. The newly acquired phenotypic variation exhibited by clonal plants has been linked to non-genetic modifications induced during the regeneration process, though the precise nature of these modifications and the factors implicated remain poorly understood. By generating clonal plants through two different methods and using two distinct tissues-roots and leaves-, we show that the phenotypic variation found in clonal plants is linked to heritable changes in DNA methylation marks already present in the founder tissues. Further, these novel phenotypes are associated with specific patterns of gene expression and metabolic changes. Our findings unveil specific pathways underpinning new phenotypic and molecular variation that arises and accumulates in clonal plant populations.

• Dokumententyp: Zeitschriftenartikel
• Fakultät: Biologie
• Themengebiete: 500 Naturwissenschaften und Mathematik > 570 Biowissenschaften; Biologie
• ISSN: 1553-7404
• Sprache: Englisch