Segregation of an MSH1 RNAi transgene produces heritable non-genetic memory in association with methylome reprogramming

Xiaodong Yang, Robersy Sanchez, Hardik Kundariya, Tom Maher, Isaac Dopp, Rosemary Schwegel, Kamaldeep Virdi, Michael J. Axtell and Sally A. Mackenzie ()
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Xiaodong Yang: The Pennsylvania State University
Robersy Sanchez: The Pennsylvania State University
Hardik Kundariya: The Pennsylvania State University
Tom Maher: The Pennsylvania State University
Isaac Dopp: The Pennsylvania State University
Rosemary Schwegel: The Pennsylvania State University
Kamaldeep Virdi: University of Nebraska
Michael J. Axtell: The Pennsylvania State University
Sally A. Mackenzie: The Pennsylvania State University

Nature Communications, 2020, vol. 11, issue 1, 1-17

Abstract: Abstract MSH1 is a plant-specific protein. RNAi suppression of MSH1 results in phenotype variability for developmental and stress response pathways. Segregation of the RNAi transgene produces non-genetic msh1 ‘memory’ with multi-generational inheritance. First-generation memory versus non-memory comparison, and six-generation inheritance studies, identifies gene-associated, heritable methylation repatterning. Genome-wide methylome analysis integrated with RNAseq and network-based enrichment studies identifies altered circadian clock networks, and phytohormone and stress response pathways that intersect with circadian control. A total of 373 differentially methylated loci comprising these networks are sufficient to discriminate memory from nonmemory full sibs. Methylation inhibitor 5-azacytidine diminishes the differences between memory and wild type for growth, gene expression and methylation patterning. The msh1 reprogramming is dependent on functional HISTONE DEACETYLASE 6 and methyltransferase MET1, and transition to memory requires the RNA-directed DNA methylation pathway. This system of phenotypic plasticity may serve as a potent model for defining accelerated plant adaptation during environmental change.

Date: 2020
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DOI: 10.1038/s41467-020-16036-8

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