Review

Tansley insight
Fruit development and epigenetic modifications

Author for correspondence: Dengguo Tang1, Philippe Gallusci2 and Zhaobo Lang1
Zhaobo Lang 1
Tel: +86 21 57078250 Shanghai Center for Plant Stress Biology, National Key Laboratory of Plant Molecular Genetics, Center of Excellence in Molecular
Email: zblang@psc.ac.cn Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China; 2Laboratory of Grape Ecophysiology and Functional Biology,
Received: 5 March 2020 Bordeaux University, INRAE, Bordeaux Science Agro, Villenave d’Ormon 33140, France
Accepted: 1 May 2020

Contents

Summary 839 IV. Perspectives 842

I. Introduction 839 Acknowledgements 843

II. DNA methylation in fruit development and ripening 840 References 843

III. Histone modifications and fruit development 842

New Phytologist (2020) 228: 839–844
doi: 10.1111/nph.16724
Key words: DNA methylation, epiallele,
histone modifications, fruit development, fruit
ripening.
Summary
Fruit development is a complex process that is regulated not only by plant hormones and
transcription factors, but also requires epigenetic modifications. Epigenetic modifications include
DNA methylation, histone post-translational modifications, chromatin remodeling and non-
coding RNAs. Together, these epigenetic modifications, which are controlled during develop-
ment and in response to the environment, determine the chromatin state of genes and contribute
to the transcriptomes of an organism. Recent studies have demonstrated that epigenetic
regulation plays an important role in fleshy fruit ripening. Dysfunction of a DNA demethylase
delayed ripening in tomato, and the application of a DNA methylation inhibitor altered ripening
process in the fruits of several species. These studies indicated that manipulating the epigenome
of fruit crops could open new ways for breeding in the future. In this review, we highlight recent
progress and address remaining questions and challenges concerning the epigenetic regulation
of fruit development and ripening.

researchers have demonstrated that plant hormones and transcrip-

I. Introduction
Angiosperms are characterized by the development of a specific
organ, the fruit. Fruits can be divided into dry types (e.g.
Arabidopsis and almond fruits) and fleshy types (e.g. tomato and
apple fruits). The development and ripening of fleshy fruits are
characterized by a range of cellular, metabolic and molecular
changes, including cell division and elongation that ensure fruit
growth, softening, and accumulation of pigments, soluble sugars
and aromatic volatiles (Klee & Giovannoni, 2011; Seymour et al.,
2013). Furthermore, fleshy fruits can be divided into two
subclasses: climacteric fruits (e.g. tomato and banana fruits) that
require a burst of respiration and ethylene production for ripening
to occur and nonclimacteric fruits that do not (e.g. strawberry and
sweet orange fruits) (Seymour et al., 2013). In the last few decades,
tion factors are key factors controlling the development and
ripening of both climacteric and nonclimacteric fruits (Jiang & Fu,
2000; Adams-Phillips et al., 2004; Giovannoni, 2004, 2007;
Pandolfini et al., 2007). In addition, there is increasing evidence
that epigenetic regulators also play critical roles in fruit develop-
ment and ripening, and that they might work together with
hormones and transcription factors (Seymour et al., 2008, 2013;
Klee & Giovannoni, 2011; Teyssier et al., 2015; Gallusci et al.,
2016; Giovannoni et al., 2017; Lang et al., 2017; Bucher et al.,
2018). Epigenetic modifications are defined as ‘mitotically and/or
meiotically heritable changes in genome activity that are not caused
by genomic DNA sequence changes’ (Goldberg et al., 2007;
Eichten et al., 2014). They include DNA methylation, histone
post-translational modifications (HPTMs, e.g. histone acetylation,

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840 Review Tansley insight
histone methylation), histone variants (e.g. H2A.Z, H3.3) and
noncoding RNAs (Hsieh & Fischer, 2005) that can interact with
each other to determine specific chromatin states, thereby activat-
ing or repressing gene expression (Du et al., 2015).
Although early epigenomic studies were limited to the model
plant Arabidopsis, the increasing number of horticultural plant
genomes that have recently been sequenced and assembled,
together with the development of new technologies, has facilitated
the study of epigenetic modifications in crops, including fruit
crops. Most studies of epigenetic regulation of fruit development
and ripening have been performed on tomato, because tomato is
conducive to genetic transformation, has a well-assembled genome
and has many mutants with developmental defects (Pesaresi et al.,
2014). However, several other fruit crops, such as strawberry and
sweet orange, now have been analyzed, leading to a complex view of
the possible roles of epigenetic regulations in fruits (Manning et al.,
2006; Teyssier et al., 2008; Zhong et al., 2013; Liu et al., 2015;
Lang et al., 2017; Cheng et al., 2018; L€ u et al., 2018; Huang et al.,
2019). In this report, we discuss current state of the art concerning
the possible roles of epigenetic regulations in fleshy fruit develop-
ment and ripening.
II. DNA methylation in fruit development and ripening
In both mammals and plants, DNA methylation is a conserved but
reversible epigenetic modification that usually involves the addition
of a methyl group to the fifth carbon of the cytosine ring. Four
processes regulate DNA methylation in plants: de novo DNA
methylation, DNA methylation maintenance, active DNA
demethylation and passive DNA demethylation (Zhang et al.,
2018; Liu & Lang, 2020). In Arabidopsis, de novo methylation is
mediated by the RNA-directed DNA methylation (RdDM)
pathway (Matzke & Mosher, 2014). By contrast, DNA methyla-
tion maintenance depends on DNA methyltransferase 1 (MET1),
chromomethylase 3 (CMT3), CMT2 and the RdDM pathway
(Law & Jacobsen, 2010; Zhang et al., 2018). Active DNA
demethylation in plants is mediated by Repressor of Silencing 1
(ROS1) family proteins, which are 5-mC DNA glycosylases/lyases
(demethylases) (Gong et al., 2002; Gehring et al., 2006; Ortega-
Galisteo et al., 2008). The DNA methylation pattern is determined
by the antagonistic activities of DNA methylation and
active demethylation (Tang et al., 2016; Zhang et al., 2018). A
change in the balance between DNA methylation and active
demethylation will alter the DNA methylation status of the genome
(Fig. 1a).
Loci-specific changes in DNA methylation associated with
fruit development and ripening
Hadfield et al. (1993) did the pioneering work that found the loss of
DNA methylation at promoters of ripening-specific genes during
ripening. Early evidence that DNA methylation affects fruit
ripening was provided by the characterization of the tomato variant
Colourless non ripening (CNR), which showed an inhibition of fruit
softening and an absence of carotenoid and flavor compound
accumulation(Manning et al., 2006). The Cnr phenotype was due
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to the hypermethylation of the 286 bp region located 2.4 kb
upstream of a SQUAMOSA promoter binding protein-like (SBP
box/SPL) transcription factor, which leads to repression of this gene
(Manning et al., 2006). More recently, naturally occurring
variations in vitamin E content in tomato fruits was associated
with changes in DNA methylation at the promoter of a 2-methyl-6-
phytylquinol methyltransferase (VTE3 (1)) gene (Quadrana et al.,
2014). Epiallelic variations at key genes were also shown to control
fruit phenotypes in several other fruit crop species. In apple and
pear fruits, for example, hypermethylation of the MYB10 promoter
region caused silencing of the MYB10 gene and as a consequence a
reduction in anthocyanin accumulation in the skin of fruits (Telias
et al., 2011; Wang et al., 2013; El-Sharkawy et al., 2015). In oil
palm (Elaeis guineensis), the hypomethylation of a Karma
transposon, which is located in the intron of EgDEF1, is responsible
for the mantled phenotype of some somaclonal variants (Ong-
Abdullah et al., 2015). These results indicated that locus-specific
changes of DNA methylation could modify fruit traits both at early
developmental stages and during ripening. Based on the findings
described above, plant breeding strategies should consider not only
genetic variation but also epigenetic variation as a source of
phenotypic variations, although the transgenerational stability of
the epigenetic variation could be a concern.
Genome-wide DNA methylation dynamics during fruit
development and ripening
Teyssier et al. (2008) provided initial evidence of the dynamic
change in DNA methylation during fruit development. They
reported a global decrease in DNA methylation in the pericarp of
tomato fruit during ripening. Later, Zhong et al. (2013) performed
whole-genome bisulfite sequencing (WGBS) in tomato fruits at
four developmental stages and confirmed the genome-wide loss of
DNA methylation during ripening. Additionally, treatment of
immature fruits with 5-azacytidine, a DNA methylation inhibitor,
induced premature ripening, demonstrating a causal relationship
between methylation level and ripening induction (Zhong et al.,
2013).
Mechanistic insight into the global loss of DNA methylation
during tomato fruit development was provided by studies of
SlDML2 (Liu et al., 2015; Lang et al., 2017). SlDML2, an ortholog
of the Arabidopsis AtROS1, encodes a tomato DNA demethylase,
and knockdown or knockout of SlDML2 dramatically delays
ripening (Liu et al., 2015; Lang et al., 2017). Using WGBS to
analyze the methylation landscape in fruits of the sldml2 mutant led
to the demonstration that the ripening-induced expression of
SLDML2 is necessary for the global loss of DNA methylation
during ripening (Lang et al., 2017) (Fig. 1b). Transcriptome
analysis suggested that SlDML2 is involved in the regulation of
genes involved in carotenoid, ethylene biosynthesis and ethylene
signaling, and in the expression of known ripening-associated
transcription factors (Liu et al., 2015; Lang et al., 2017), including
the MADS-box transcription factor RIPENING INHIBITOR
(RIN), an essential regulator of fruit ripening (Vrebalov et al.,
2002; Ito et al., 2017). Many RIN-targeted genes are hypomethy-
lated in their promoter regions during ripening (Zhong et al.,
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(a)
Methylation Demethylation

Balanced before ripening

Ri

Ripening
g pe
nin nin
R ipe g

(b) Tomato (c) Strawberry (d) Sweet orange

Methylation Demethylation Methylation Demethylation Methylation Demethylation

DML2 RdDM Demethylase

upregulated downregulated downregulated
Whole-genome hypomethylation Whole-genome hypomethylation Whole-genome hypermethylation

Fig. 1 Changes in the balance between DNA methylation and demethylation during fruit development. (a) The activities of methylation and demethylation
reactions are balanced during early fruit development. (b) The balance is disrupted in tomato fruits during ripening. With the increased expression of SlDML2,
tomato fruits undergo whole-genome hypomethylation, which promotes ripening. (c) Due to the downregulation of RdDM pathway genes during fruit
development, strawberry fruits also undergo whole-genome hypomethylation during ripening. (d) Sweet orange fruits undergo whole-genome
hypermethylation during development and ripening due to the reduced expression of demethylation genes.

2013). These results suggested that transcription factors and DNA
methylation interact to regulate fruit development. The crosstalk
among DNA methylation, hormone pathways and transcription
factors requires further investigation.
More recently, Zhou et al. (2019) described that SlALKBH2, an
RNA demethylase gene, mediated the ripening-associated dynam-
ics of mRNA m6A methylation in tomato, and affected fruit
ripening through regulating the stability of SlDML2 mRNA.
In addition to active DNA demethylation, the roles of DNA
methylation pathways in fruit development have also been studied.
Gouil & Baulcombe (2016) found that the RdDM-knockout
mutants slnrpd1 were defective in the development of leaves,
flowers and fruits, and that the slnrpe1 mutant was lethal. Yang et al.
(2019) reported that knockout mutants of SlMET1 in tomato were
defective in the development of leaves and inflorescences, and
displayed parthenocarpy. These studies indicated that the RdDM
pathway and SlMET1 have critical roles in vegetative and
reproductive growth and fruit development in tomato.
Indeed, tomato is a model organism for the study of climacteric
fruit development. The question arises as to whether the
mechanisms identified in tomato are also operating in other fruits.
To address this question, Cheng et al. (2018) profiled the DNA
methylomes of the nonclimacteric strawberry fruit, and demon-
strated that as observed in tomato fruits, strawberry fruits undergo
whole-genome DNA hypomethylation during ripening. However,
this global loss of DNA methylation in strawberry fruits is due to a
weakened RdDM pathway rather than to the induced expression
of DNA demethylase genes (Fig. 1c). Cheng et al. (2018) also
found that the application of a DNA methylation inhibitor caused
early ripening of strawberry fruits. In another study, Huang et al.
(2019) found unexpectedly that DNA methylation in sweet orange
fruits increased during ripening, which was opposite to observa-
tions in tomato and strawberry. The authors then showed that the
whole-genome DNA hypermethylation during sweet orange fruit
development was associated with the decreased expression of DNA
demethylase genes (Fig. 1d), and that application of a DNA
methylation inhibitor delayed ripening. The ripening-associated
methylomes have also been profiled in apple, banana, melon,
papaya, peach, pear, cucumber, grape and watermelon (L€ u et al.,
2018). From an evolutionary perspective, the results indicated that
the direction of change (loss or gain) of DNA methylation varies
between these species, therefore confirming the observation
performed in strawberry, tomato and sweet orange. Interestingly,
whatever the types of methylation changes, interfering with DNA
methylation was shown to interfere with normal ripening in all
fruit crops tested to date, including tomato, strawberry and sweet
orange (Zhong et al., 2013; Liu et al., 2015; Lang et al., 2017;
Cheng et al., 2018; Huang et al., 2019), indicating that DNA
methylation plays a crucial role in fruit ripening, but which may
vary between species.
III. Histone modifications and fruit development
Recent evidence suggests that the histone modifications also
participate in the regulation of fruit development and ripening Guo
et al., 2017a,b, 2018). The histone acetylation mark is usually
associated with gene activation and is a reversible mark that is
controlled by the balanced activity between histone

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acetyltransferases (HATs) and histone deacetylases (HDACs)
(Wolffe & Pruss, 1996; Annunziato & Hansen, 2000; Roth
et al., 2001; de Ruijter et al., 2003). Although several studies have
now shown that various histone modifiers present enhanced or
specific expression in fruits (reviewed by Gallusci et al., 2016),
functional data are limited to the study of HDACs and polycomb
group proteins in tomato (Fig. 2) (How Kit et al., 2010; Boureau
et al., 2016; Guo et al., 2017a,b, 2018). Indeed, HDACs seem to
have contrasted function in fruits, as knockdown of a tomato
HDAC, SlHDT3, resulted in delayed tomato fruit ripening and
limited carotenoid accumulation (Guo et al., 2017a). By contrast,
the knockdown of two other HDACs, SlHDA1 and SlHDA3,
resulted in earlier ripening and increased carotenoid accumulation
(Guo et al., 2017b, 2018). Hence HDACs are probably involved in
Histone acetylation
SIHDT3 (Guo et al., 2017a)
SIHDA1/SIHDA3 (Guo et al., 2017b, 2018)
the fine tuning of gene expression during ripening and in the
kinetics of ripening. Whether they are key elements involved in
ripening induction is unclear.
A few studies have investigated the role of the Polycomb
Repressive Complex 2 complexes (PRC2s) in fruits. PRC2s are
responsible for the trimethylation of histone H3 at Lys27
(H3K27me3), a repressive epigenetic mark that is important in
developmental transitions (Kassis & Brown, 2013; Mozgova &
Hennig, 2015; F€orderer et al., 2016). The RNAi lines of SlEZ1, a
gene encoding PRC2 protein Enhancer of zeste (E(z)) in tomato,
had an increased number of fruit locules (How Kit et al., 2010), and
knockdown of SlEZ2 altered fruit shape, texture and color
(Boureau et al., 2016). More recently, the fruit ENCODE data
revealed that H3K27me3 is a conserved epigenetic mark that is
associated with fruit ripening during plant evolution. In leaves and
immature fruits of all plants examined in this project, H3K27me3
was deposited at ethylene biosynthesis or ripening regulator genes,
where it suppresses ripening. At the onset of ripening, H3K27me3
was removed from these regions, suggesting that removal of this
repressive mark might be necessary for ripening induction (Fig. 2)
(L€u et al., 2018). However, how H3K27me3 contributes to
ripening-associated gene regulation remains unclear. In addition,
how histone modification and DNA methylation cooperate to
regulate ripening-associated gene expression requires further
investigation.

Tomato fruit IV. Perspectives

ripening Fruit development is a complex process that involves both genetic
and epigenetic regulations, and is affected by environmental
factors. In this review, we have summarized the most recent research
on the epigenetic mechanisms governing fruit development and
SIEZI/SIEZ2 (How Kit et al., 2010; ripening. During fruit ripening, a global change of DNA
Boureau et al., 2016) methylation has been documented in all examined fruit species,
H3K27me3 (Lü et al., 2018) although the direction of change (loss or gain) is not conserved
among species. The overall process of fruit development and
ripening is in many ways similar to the development and aging
Histone methylation process in animals and humans, such as the active cell division in
early stages and cell senescence in later stages. Interestingly, a
Fig. 2 Roles of histone acetylation and methylation in tomato fruit ripening. number of studies have recently demonstrated that epigenetic
Several studies have shown that histone acetylation and methylation regulation participates in animal and human aging (Pal & Tyler,
activities play important roles in tomato fruit ripening. 2016; Sen et al., 2016; Cheng et al., 2017; Sidler et al., 2017). For

DNA
methylation

Natural
Histone epialleles
modification
Epigenetic Fruit yield Superior
modifications and quality fruit crops
Chromatin Fig. 3 Utilizing epigenetic variations to
remodeling Induced improve fruit crops. Natural or induced
epialleles changes in epigenetic marks including DNA
methylation, histone modifications, chromatin
Non-coding remodeling and noncoding RNAs may lead to
RNAs the formation of epialleles, which could be
used to breed superior fruit crops.

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example, several reports have documented age-dependent global
DNA hypomethylation and locus-specific hypermethylation
(Bjornsson et al., 2008; Bollati et al., 2009; Heyn et al., 2012;
Jung & Pfeifer, 2015; Bormann et al., 2016). These results
suggested that aging in both fruits and mammals is accompanied by
a change in the balance between DNA methylation and demethy-
lation pathways, leading to a global change in DNA methylation
(Fig. 1a–d). Epigenetic regulation in general may represent a
conserved mechanism that affects aging or cellular senescence in
animals, humans and higher plants.
More importantly, epigenetic modifications could be highly
valuable for crop improvement, providing a source of phenotypic
variations (Gallusci et al., 2017). Hence, manipulating the
epigenome of fruit crops could open new ways for breeding in
the future. Either epimutants/variants or deactivated CAS9-
methylase or -demethylase fusion-mediated site-specific epigenetic
modification could be used to generate superior epialleles for crop
improvement (Fig. 3) (Xu et al., 2019).
Despite recent progress, many important questions remain
concerning our understanding of epigenetic regulations of fruit
development: Which signals trigger the epigenetic changes
during ripening? How are epigenetic regulators specifically
recruited to ripening-associated loci? What are the molecular
mechanisms underlying the crosstalk among plant hormones,
transcription regulators and epigenetic modifications in the
regulation of fruit development and ripening? In summary, the
epigenetic regulation of fruit development and ripening is a
crucial and exciting research area with many challenges and
unanswered questions.
Acknowledgements
This work was supported by the National Key Research and
Development Program (2018YFD1000200) and Strategic Priority
Research Program of the Chinese Academy of Sciences (Grant
XDB27040000) (to ZL).
ORCID
Zhaobo Lang https://orcid.org/0000-0002-0269-8663
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