Epigenetic modification for horticultural plant improvement comes of age

Highlights

• Epigenetic modifications act as repressive or active regulators in modulation of gene expression in plants.

• Essential roles of DNA and histone modifications have been revealed in development processes and response to environmental factors.

• Emerging RNA modifications are crucial to control fruit ripening and grafting in plants.

• Evidence of epigenetic regulation supports further studies on functional genomics and breeding applications in horticultural plants.

Abstract

Our era has witnessed tremendous technique advances and mechanically epigenetic improvement in plant epigenetics, mainly including histone post-translational modifications (PTMs) and DNA methylation, which have been characterized as playing vital roles in development processes and plant response to environmental factors. Recently, chemical modifications on RNAs like 5-methylcytosine (m⁵C) and N6-methyladenosine (m⁶A) have been revealed as a new layer of epigenetic marks to regulate gene translation efficiency in model plant Arabidopsis thaliana and with later discovery of horticultural species like tomato (Solanum lycopersicum) and poplar (Populus trichocarpa). In model plants, these epigenetic modifications on DNA, RNA, and histone tails largely trigger innumerable studies on how epigenetic mechanisms are involved in gene regulation and biological functions. As an emerging research field in horticultural plants, epigenetic modifications have bloomed in fruit development and ripening, grafting, and bud dormancy. In this Review, we have demonstrated recent advances of high-throughput sequencing methods, summarized epigenetic enzymatic systems to install, remove and recognize epigenetic marks, discussed essential roles of epigenetic regulation, and proposed how innovative computation techniques like machine learning and deep learning are set to understanding epigenetic regulation mechanisms in horticultural plants. We also raise future perspectives on how epigenetic modifications act as new additions for understanding their roles in gene expression that is required for development and environmental adaptation in horticultural plants.

Introduction

Alterations in the nucleotides sequence cause to change in the activity and function of a gene by forming a specific protein for cell functionality is termed as “Genetics”. In contrast, “Epigenetics” as extra regulatory layer provides instructions where, when and how to regulate gene expression. The genetic information in all cell types of an organism is identical (Allis and Jenuwein, 2016; Goldberg et al., 2007). However, all the genes are not expressed simultaneously by all cell types; Instead, all cells in higher organisms possess the same genetic information, but only limited and specific set of genes is expressed by every cell, that describes the cell type. This exciting phenomenon is accomplished the by a variety of pathways which are combine termed as the genetics and epigenetics, that lead to heritable and stable changes in the gene expression patterns during developmental cues and response to environmental stimuli in both animals and plants (Cavalli and Heard, 2019; Schuettengruber et al., 2017).

The epigenetic mechanism in plants is mainly regulated by four precise mechanisms including DNA 5-methylcytosine (5mC) and DNA N6-methyldeoxyadenosine (6mA), histone posttranscriptional modifications (PTMs), chromatin remodeling, and non-coding RNAs (ncRNAs) (Fig. 1). These mechanisms are accomplished by different families of enzymatic proteins that act to catalyze or install (termed as “writers”), to remove (termed as “erasers”), and to interpret (termed as “readers”) the epigenetic modifications to nucleic acids or histone tails (Fig. 2A). Among these modifications, DNA 5mC and histone PTMs are the most commonly studied epigenetic marks responsible for regulating numerous cellular pathways along with gene expression to control several developmental signals and environmental adaption in plants (Feng et al., 2010; Liu et al., 2010; Pu and Sung, 2015; Smith and Meissner, 2013; Zhang et al., 2018a). They are involved in the regulation of flowering time (He, 2012), fruit ripening (Gallusci et al., 2016; Liu et al., 2015), seed and endosperm development (Köhler and Makarevich, 2006; Zhang et al., 2021), organogenesis of the symbiotic nodule (Satgé et al., 2016), parental imprinting (Iwasaki and Paszkowski, 2014; Zhang et al., 2012), and maintenance and reprogramming of cell fate (Birnbaum and Roudier, 2017; Xiao and Wagner, 2015). Besides 5mC and histone PTMs, recent discovery of RNA modifications like RNA 5-methylcytosine (m⁵C) and RNA N6-methyladenosine (m⁶A) have been regarded as new layers of epigenetic regulation on plant development and environmental responses (Liang et al., 2020b; Shen et al., 2019; Zhang et al., 2020b).

In horticultural plants, recently, accumulating studies have revealed that epigenetic modifications play significant roles in controlling the growth, development and environmental responses (Agustí et al., 2020; Cheng et al., 2018; Liao et al., 2021; Tang et al., 2020; Zhang et al., 2020c; Zhou et al., 2019). Compared to epigenetic regulation mechanisms in model plants, although studies have reveled associations with gene regulation and biological functions in horticultural plants, we are still at the early stage on understanding the mechanisms controlled by epigenetic modifications. However, we are now firmly entering in the ‘Big Data’ era of genomics in horticultural plants (Chen et al., 2019), and it seems to be that there are good reasons to explore epigenetic and epigenomic studies and approaches that can likely broaden our understanding of gene regulation and biological functions in horticultural plants. As an emerging research field in horticultural plants, epigenetic modifications have bloomed in fruit development and ripening, grafting, and bud dormancy.

In this Review, we have discussed recent advances of high-throughput sequencing (HTS) methods, concluded epigenetic enzymes (writers, erasers, and readers), and then demonstrated essential roles of epigenetic regulation in horticultural plant development. We also propose future perspectives of epigenetic modifications for understanding of their roles to regulate gene expression and biological functions in horticultural plants.