The complex world of genetic systems for elaborate gene regulation that enables flexible plant life

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Despite being sessile organisms, plants survive and reproduce in every corner of this planet, from arid deserts to tropical rainforests to Antarctica. Understanding the molecular and genetic mechanisms that enable plants to adapt to such a wide variety of environments will be of utmost interest toward the preservation of biodiversity and food security. One of the unique features of plants is the remarkable ability to adapt their developmental programs to surrounding environments, which is partly because they continue to make new organs after embryogenesis. Molecular genetic research using model plants like Arabidopsis thaliana or rice (Oryza sativa) has revealed the elaborate mechanisms that sustain plants’ flexible development and responses to these varied environments.

In this issue of Genes and Genetic Systems, Reina Komiya, Nobutoshi Yamaguchi and I review the emerging fields of the control of biological phenomena – such as development, reproduction, and stress response and memory – via chromatin- or RNA-based mechanisms in plants. Ever since the discovery of Mendelian inheritance in Gregor Mendel’s experiments with pea plants, plants have been serving as models of genetic studies and pioneering the discovery and characterization of conserved molecular mechanisms such as small RNA-mediated regulation of gene expression (e.g., co-suppression and RNA interference) and epigenetic regulation. Komiya summarizes the functions and regulation of a unique type of small interfering RNA, called phased small interfering RNA (phasiRNA), found in land plants. Processing of more than 1,300 long non-coding RNAs produces various phasiRNAs during reproductive development in rice, and Komiya and her colleagues recently discovered that these phasiRNAs play a crucial role in anther development, using genome editing and detailed imaging analyses. Moreover, they found that the sterile phenotype of a phasiRNA-defective mutant is dependent on photoperiod. She discusses the role and detailed mechanism of action of this enigmatic short non-coding RNA species.

I summarize the recent progress on epigenetic regulation, focusing on the counteraction between silencing and anti-silencing factors mainly in gene bodies (i.e., the transcribed region of genes), and discuss the potential implication of these mechanisms in the adaptation of plants to fluctuating environments. While characterizing regulators of histone modifications, my colleagues and I found dynamic and plastic features of epigenome regulation and their potential contribution to environmental adaptation, such as pathogen responses. We also recently found a connection between epigenome regulation and non-coding transcription in the antisense direction relative to coding genes, the underlying mechanism of which has a crucial role in genome maintenance and plant responses to seasonal fluctuations of temperature. Focusing on the plastic nature of epigenome regulation has begun to illuminate the biological functions of the epigenome, which will be elucidated in the future.

Yamaguchi describes an emerging hot topic in plant biology, stress memory. Without a brain or nervous system, how plants are able to memorize past stress and utilize that information to better cope with future stress is an intriguing question to be answered using molecular genetics and (epi)genomic research. Yamaguchi and his colleagues recently discovered that A. thaliana plants that experience mild heat stress “remember” the experience for several days and withstand subsequent harsher temperature. Using genetic and epigenomic analyses, they showed that a sustained reduction of the repressive histone mark H3 lysine 27 trimethylation in two key heat stress response gene regions is responsible for the heat memory. He discusses this and other chromatin- and/or RNA-based mechanisms that allow plants to memorize temperature information.

I hope that the plant molecular genetics studies reviewed here will shed light on the paths toward better interactions between plants and humans under global warming and associated environmental changes. In addition, I would like to mention that understanding the complex genetic systems that provide flexibility to plant life is a promising research field in fundamental biology.