Download Genetic Imprinting in Maize Bhavani P1*, Harinikumar K. M1

Genetic Imprinting in Maize
Bhavani P1*, Harinikumar K. M1, Shashidhar H. E1and Sajad Majeed Zargar2
1
Department of Biotechnology, University of Agricultural Sciences, GKVK, Bangalore, Karnataka560065, India, 2 School of Biotechnology, Sher-e-Kashmir University of Agricultural Sciences and
Technology of Jammu, Chatha, Jammu, J&K-180009 India
*Corresponding author: [email protected]
Abstract
Genetic imprinting is the epigenetic phenomenon observed in flowering plants
including maize in which, an allele shows differential expression depending on the
parent it is inherited. Imprinted genes are modified during gametogenesis so that
only paternal or maternal allele is expressed after fertilization. This review focuses
on the major processes involved in the regulation of imprinting like DNA
methylation, covalent modifications of histones and chromatin remodeling citing
examples of maize. This review also summarizes theimprinted genes that have
been reported in maize including Fie1, Fie2, Peg1, Nrp1, Mez1, Meg1, Mee1, VIP5
and Yuc8.
Keywords: Maize, genetic imprinting, epigenetics, histone methylation
Introduction
Transfer of acquired characters of an individual within the lifetime without the change
in DNA sequence in termed as “epigenetics” unlike Mendelian genetics, which
describes the inheritance of genes that encode specific traits (Ho and Burggren, 2010).
Though, the “theory of acquired inheritance” was given by Lamarck way back in 1809
and endorsed by Lysenko (Lysenko, 1948). The concept did not gain much needed
attention due to the more convincing evidence obtained by the experiments of Mendel
and predecessors (detailed in Weldon, 1902). But inheritances of certain traits like
veliger development in snail (Freeman and Lundelins, 1982), epigenetic abberrations
and spermatogenesis (Singh et al., 2011), impact of exposure of parents to
environmental stress on development of resistance to the environment stress in the
progeny (Agrawal et al., 1999) has opened up a new dimension of this, much ignored
theory of science. The term “epigenetics” was first coined by Waddington
(Waddington, 1942), which literally means “above stress”. Waddington defined
epigenetics as “environment-gene interactions that induce developmental phenotype”.
But the recent and the most widely accepted definition is ‘‘an epigenetic trait is a stably
heritable phenotype resulting from changes in a chromosome without alterations in the
DNA sequence”(Singh et al., 2011). The modifications that add this extra piece of
information without changing the DNA sequences are DNA methylation, histone
modifications and chromatin remodeling proteins. Therefore, the genome is the sum
total of the information encoded by the nucleotide sequences while the epigenome is
the amassed effect of these DNA and histone modifications on gene expression without
affecting the base sequence. Thus, imprinted expression states are under epigenetic
control (Springer and Gutierrez-Marcos, 2009). These states can have short-term and
long-term effects and could be trans-generational (Anway et al., 2005).
In plants, the evidences of genetic imprinting have been observed in triploid endosperm
and not in vegetative tissues (Gehring et al., 2004; Gehring et al., 2009; Huh et al.,
2008; Jullien and Berger, 2009; Springer and Gutierrez-Marcos, 2009). Since the active
and silenced state of gene is present in the same nucleus, there is the possibility of
existence of distinct mechanisms to maintain the epigenetic state between the parental
alleles. Maize (Zea mays L.) provides an excellent model to study the role of epigenetic
variation and parent-of-origin effect (Eichten et al., 2011; Waters et al., 2011) owing to
its large endosperm. Genetically, maize is a highly diverse species (Buckler et al., 2006;
Messing and Dooner, 2006) and has complex genome organization with many
interspersed genic and repetitive regions (Rabinowicz and Bennetzen, 2006; Schnable
et. al., 2009). Imprinted genes are arranged in singletons in Arabidopsis and Rice
(Gehring et al. 2011, Luo et al. 2011, Wolff et al. 2011) but gene clusters are relatively
more frequent in maize (Zhang et al. 2011), in contrast, mammals, where they are
found in clusters (Kinoshita, 2004; Gutierrez-Marcos et al. 2006; Jullien, 2006; Feil and
Berger, 2007). Imprinted gene expression is classified as paternal imprinting (PEG) or
maternal imprinting (MEG) depending upon which parental allele is expressed, allelespecific imprinting (certain alleles at a given locus are imprinted) or gene-specific
imprinting (all the alleles at a given locus are imprinted), binary imprinting
(monoallelic expression where only one of the parental allele is expressed and other is
silent) or differential imprinting (biallelic expression where both alleles are expressed
but in different quantities) and constitutive- and transient-imprinted genes depending on
the duration of imprinting (Springer and Gutierrez-Marcos, 2009). Imprinting was first
reported for R locus in maize which is responsible for aleurone pigmentation of the
maize kernel, such as R-r: standard (R-r:std) wherein maize produced fully colored
kernel when inherited from female and mottled kernels when paternally inhererited
(Kermicle, 1970; Kermicle, 1978, Kermicle and Alleman, 1978; MacDonald, 2012).
Although genetic imprinting was first discovered in maize, so far there are only seven
gene-specific imprinted genes reported in maize (including Fie1, Fie2, Peg1, Nrp1,
Mez1, Meg1, and Mee1), most of which are preferentially expressed in the endosperm.
All except Peg1 show maternal-specific expression (Zhang et al., 2011). Recent
advances in transcriptome profiling techniques like deep sequencing have reported
many PEGs and MEGs in Maize endosperm (Waters et al., 2011).
Epigenetic mechanisms
Chromatin level of genome activity is controlled at various levels of DNA and histone
modifications (Roudier et al, 2011). Covalent modifications of histones, DNA
methylation, incorporation of histone variants, and other factors, such as chromatinremodelling enzymes or small RNAs, all contribute to defining distinct chromatin states
that modulate access to DNA (Berger, 2007; Kouzarides, 2007; Roudier et al, 2011).
The different epigenetic mechanisms include:
a. Modification at the DNA level (Cytosine methylation)
b. Modifications at protein level - the histone code (Histone acetylation, Histone
methylation, Histone phosphorylation, Histone ubiquitination, Different types of
histones)
c. Chromatin remodeling – chromatin remodeling proteins
DNA methylation
Methylation patterns of the cytosine residues in the CpG islands serve as one of the
important source code in regulating gene expression in epigenetic mechanism. CpG
island is a stretch of DNA sequence with high frequency of CpG occurrence and C + G
content of more than 50% (Gardiner-Garden and Frommer, 1987;Takai and Jones,
2002) and most commonly observed near promoter regions (Bird et al., 1995).
Hypermethylation of DNA in CpG islands is associated with the maintenance of gene
suppression, while hypomethylation in these regions is associated with gene expression
(Biermann and Steger, 2007). DNA methylation is regulated by DNA
methyltransferases that transfer methyl groups from S-adenosyl-methionine to 5’
position of cytosine residues of CpG island (Biermann and Steger, 2007). In plants,
DNA methylation occurs at cytosine residues in CG, CHG and CHH different sequence
contexts (Law and Jacobsen, 2010). Unlike DNMT1 which is involved in maintaining
established methylation patterns and DNMT3A and DNMT3B in de novo methylation
patterns in mammals (Bestor et al., 1988, Lei et al., 1996, Okano et al., 1999, Singh et
al., 2011), while maintenance is carried out by DNA methyltransferase 1 (MET1),
variant in methylation (VIM) and decreased DNA methylation 1 (DDM1)(at CG sites),
chromomethylase 3 (CMT3) (CHG and CHH) and to some extent de novo CHG
methylation is established by domains rearranged methyltransferase 2 (DRM2) in
plants (Law and Jacobsen, 2010, Wollmann and Berger, 2012). Twenty-four nucleotide
long (24 nt) small interfering RNAs (siRNAs) have shown to mediate De novo DNA
methylation through the RNA-directed DNA methylation (RdDM) pathway (Simon and
Meyers, 2010). The DNA glycosylase DEMETER (DME) actively removes DNA
methylation (Choi et al., 2002; Kinoshita et al., 2004) and might contribute to the
derepression of genes (Wollmann and Berger, 2012). DNA demethylation can also
occur passively in the absence of enzymes involved in methylation maintenance
process (Hauser et al., 2011). In plant endosperm and mammalian embryo, many
differentially methylated regions (DMR) are present in the Imprint Control Regions
(ICR) that has critical role in epigenetic regulation of imprinted domains (MacDonald,
2011). The methylation pattern of these DMRs are erased in germline, re-established
during gametogenesis and maintained throughout the development and lifecycle.
Further, DNA methylation is coordinated by the position and composition of
nucleosomes and associated histone modifications at genome level (Hauser et al.,
2011).
Histone modification
The chromatin is made up of nucleosome unit, which is composed of 146 bp and
wrapped around an octamer of core histones (H2A, H2B, H3 and H4) and linked by
H1. The chemical modifications of the amino acid residue present in the N-terminal tail
of these histones result in the regulation of the genes. The modifications viz.,
methylation, acetylation, phosphorylation, ubiquitylation and sumoylation at the histone
tails constitute histone code (Peterson and Laniel, 2004). There are eight common
histone modifications that are associated with active or repressed transcriptional state of
chromatin (Huan and Springer, 2008). Modifications of histones H3 and H4, especially
acetylation and methylation of histone lysine residues at N-terminal tails that protrude
from the nucleosome are best understood in terms of gene regulation (Hauser et al.,
2011).
Histone methylation is the most prominent of the post-translational
modification and is monitored by the histone methyltransferases (HMTs). HMTs are
involved in either addition or deletion of one or two methyl groups from arginine and
lysine residues (Singh et al., 2011). Histone methylation is most commonly associated
with the gene silencing, methylation of H3K9 is found in heterochromatin and silenced
promoters (Fischle et al., 2003), but it may also associate with gene activation as in
histone H3K4 dimethylation in maternal allele of maize Mez1 and ZmFie1 (Huan and
Springer 2008). Therefore, methylation of Lys9 and Lys27 of histone H3 (H3K9 and
H3K27) are linked to heterochromatin and gene silencing, while methylation of Lys4
(H3K4) is linked to transcriptional activity (Grewal and Elgin, 2002, McDonald, 2011).
Lysine methyltransferase, G9a, is involved in mono- and dimethylation of H3K9 in
euchromatin (Tachibana et al., 2007) while LSD1 and JmjC-domain-containing
proteins are methyltransferases with lysine demethylase activity that interact with
chromatin remodeling proteins to affect chromatin condensation (Okada et al., 2007).
Acetylation is the second most important posttranslational histone modification that has
antagonistic role to DNA methylation. Increased histone acetylation at lysine residues
is mediated by histone acetyl transferases (HATs) signifies active genes and
deacetylation through histone deacetylases (HDACs) inhibit gene expression (Singh et
al., 2011). The mouse Gtl2 DMR of the silent paternal allele is hypoacetylated on H3
and H4, while the active maternal allele carries high levels of acetylation on both
histones (Carr et al., 2007). MYST1, a MYST family protein is a acetyl transferase
(HAT), which acetylates H3K16 to impact chromatin architecture (Neal et al., 2000)
while SIRT1 is a deacetylase (HDAC) that removes acetyl groups from H1, H3 and H4
(Yi and Luo, 2010). Phosphorylation of histones at serine and threonine residues and
ubiquitylation of lysine residues are associated with either activation or repression of
gene depending on the context. For example, phosphorylation is usually associated with
gene activation but gene silencing is seen when the histone variant H2AX is
phosphorylated (Fernandez-Capetillo, 2003) and ubiquitylation of histone H2A is
linked to gene silencing (Baarends et al., 2003) whereas ubiquitylation of H2B is linked
to gene activation (Zhu et al., 2005). Attachment of small ubiquitin-related modifier
proteins, termed as sumoylation is yet another process of posttranslational modification
that mediate gene silencing by recruiting HDACs and heterochromatin protein 1 (Shiio
and Eisenman, 2003).
DNA methylation and histone modifications are the two
interconnected processes in epigenetic mechanisms that influence each other’s
recruitment to the silencing complex to reinforce differential epigenetic states (Tariq
and Paszkowski, 2004; Cheung and Lau, 2005).
Chromatin remodeling
Chromatin structure is associated with the active/repressed state of a gene which is
directly influence by the DNA methylation, histone modifications and chromatin
remodeling proteins. Open state of the chromatin makes DNA accessible to
transcriptional machinery and gene expression while gene expression is repressed when
the chromatin attains more compact state of heterohromatin (Fransz and Jong, 2002).
Histone modifications may impact secondary chromatin structures through
nucleosome–DNA or nucleosome–nucleosome interactions and by neutralizing charge
in the histone N-terminal tails (Wolffe and Hayes, 1999; Carruthers and Hansen, 2000;
Wang et al., 2001; Gilbert et al., 2007). The acetylation of histones corresponds with
‘open’ chromatin and enhanced transcriptional activity (Strahl and Allis, 2000) and
acetylated histone tails increase the affinity of chromatin for bromo-domain proteins
(e.g. HATs) and promote transcriptional activation (Turner 2000). Chromatin
remodeling is mediated by the alterations in location and structure of nucleosomes by
ATP-dependent chromatin remodeling proteins (Narlikar et al., 2002; Singh et al.,
2011) (e.g. the SWITCH2 [SWI2]/SUCROSE NON-FERMENTING2 [SNF2]
complex) and histone- modifying complexes (e.g. the histone deacetylase complex
[HDAC]) (Fransz and Jong, 2002). Further, the repressive complex is maintained by the
heterochromatin-associated protein HP1 that is thought to form a repressive complex by
binding to methylated H3K9 via its chromodomain and by interacting with SUV39
(Fransz and Jong, 2002). A plant homolog of HP1, LHP1 (LIKE
HETEROCHROMATIN PROTEIN1), has been reported in Arabidopsis (Gaudin et al.,
2001).
Imprinted genes in maize
Genetic imprinting is seen in endosperm of flowering plants. During fertilization one of
two sperm cells produced by the male gametophyte through meiotic division fuses with
egg cell to form seed, the other sperm cell unites with the two central cellof same
genetic constitution giving rise to triploid endosperm (Drews and Yadegari, 2002) that
serve to nourish embryo (Fig. 1). Parental differences in DNA methylation have been
identified for the imprinted maize genes ZmFie1 (Hermon et al., 2007), ZmFie2
(Gutierrez-Marcos et al., 2006) Mez1 (Haun et al., 2007), Peg1 (Gutierrez-Marcos et al.
2003), Nrp1 (Guo et al. 2003; Haun and Springer 2008), Meg1 (Gutierrez-Marcos et al.
2004), Mee1 (Jahnke and Scholten, 2009) and VIM5 and YUC10 (Zhang et al., 2011)
(Table 1). All the reported imprinted genes are preferentially expressed in the
endosperm and all except Peg1 show maternal-specific expression (Gutierrez-Marcos,
2003). Two types of imprinting exist in maize, allele-specific imprinting as seen in R
gene (Kermicle, 1970), dzr1 gene and zein protein (Chaudhuri and Messing, 1994,
Lund et al., 1995a), alpha-tubulin (Lund et al., 1995b) and gene-specific imprinting as
in ZmFie1 (Danilevskaya et al., 2003) and Nrp1 (Guo et al., 2003). Among the maize
genes, few alleles of the R locus such as R-r: standard (R-r:std) was first reported to be
imprinted (Kermicle, 1970). This R-r:std allele is responsible for the aleurone
pigmentation of maize which shows differential expression depending on the
contributing parent (Kermicle, 1970). The paternally inherited R allele gives mottled
phenotype while maternally inherited R allele gives solid phenotype (Kermicle, 1970).
The imprinting of R allele appears to be due to differential expression of the maternal
allele in relation to paternal allele rather than silencing of paternal allele (Kermicle and
Alleman, 1990). Alpha-tubulin genes exhibit differential methylation depending on
whether it is maternal or paternal inheritance (Lund et al., 1995). Locus dzr1, a
posttranscriptional regulator of zein protein also shows allele-specific imprinted
expression (Chaudhuri and Messing, 1994).
ZmFie1 and ZmFie2 are maize orthologs of the Arabidopsis FIE gene, (GutierrezMarcos et al., 2006; Raissig et al., 2011). ZmFie1 is imprinted in the endosperm, which
shows maternal expression, and paternal expression is completely absent throughout
seed development, which is repressed by DNA methylation of CpG island
(Danilevskaya et al., 2003; Gutierrez-Marcos et al., 2006; Huan and Springer; 2008).
No-apical meristem (NAM) related protein1 (Nrp1), a transcription factor, displayed
gene-specific imprinting and expressed only in endosperm (Guo et al., 2003). Janhnke
and Scholten, 2009 has shown the imprinting of maternally expressed in embryo 1
(mee1) gene of maize in both the embryo and endosperm indicating the correlation of
parent-of-origin-specific expression with differential allelic methylation. This
differential methylation is maintained in the endosperm, whereas the embryonic
maternal allele is demethylated on fertilization and remethylated later in
embryogenesis. Maternally expressed gene1 (meg1), which is a maize endosperm
transfer cell-specific gene shows maternal parent-of-origin expression pattern during
early stages of endosperm development but biallelic expression at later stages
(Gutierrez-Marcos et al., 2004). Polycomb group (PcG) proteins, Maize Enhancer-ofzeste 1(Mez1) is imprinted while Mez2 and Mez3 are not. Mono-allelic expression of
maternal Mez1 was seen in the developing endosperm and was found to be present
throughout the development of endosperm. (Huan et. al., 2009). Differentially
methylated region was found at the transcription start site of Mez1 and CpG and
CpNpG nucleotides were heavily methylated on the non-expressed paternal allele while
maternal allele showed less methylation (Huan et. al., 2007). Recent advances in
transcriptome profiling techniques like deep sequencing have reported many PEGs and
MEGs in Maize endosperm (Wang et al., 2009). Waters et al., (2011) reported 100
putative imprinted genes in maize endosperm, including 54 maternally expressed genes
(MEGs) and 46 paternally expressed genes (PEGs) using genome-wide allele-specific
expression profiling. Zhang et al., showed 179 genes (1.6% of protein-coding genes)
expressed in the endosperm to be imprinted, with 68 of them showing maternal
preferential expression and 111 paternal preferential expressions. Zhang et al., (2011)
has identified two PEGs VIM5 and Yuc10 in maize.
Conclusion and our views
Genetic imprinting is observed only in the triploid endosperm of the angiosperms in the
plant kingdom and around twelve imprinted genes have been reported in maize.
Hundreds of imprinted genes are being added to the list through deep sequencing
technologies, but the functional role is yet to be elucidated. DNA methylation and
histone modifications are the two important process involved in exertion and
maintenance of imprinting. Genetic imprinting is found to have major role in many key
developmental processes and genome dosage is one of the factors contributing to the
imprinting. Genome dosage has reported to have direct implication on the seed size in
maize. Though we can speculate that the role of imprinting in the maintenance of the
genome dosage imbalance in the cross-pollinated plants, its role in self-pollinated
plants is yet to be discerned. To date, the scientific community is still debating on its
role in evolution and significance in the process of crop improvement. Advanced
technologies like genome-wide approaches may contribute in helping the researchers to
unravel the potential mechanism of genetic imprinting and its possible benefits to crop
improvement.
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Table 1: Imprinted genes in maize and their expression pattern
Allele-specific
genes
R
Dzr-1
Zein
Alpha-tubulin
Locusspecific
imprinted
genes
ZmFie1
imprinted
Tissue-specific
expression
Endosperm
Endosperm
Endosperm
Endosperm
Tissue-specific
expression
Reference
Maternal
Endosperm
ZmFie2
Maternal
Endosperm
Nrp1
Peg1
Meg1
Mez1
Mee1
Maternal
Paternal
Maternal
Maternal
Maternal
Endosperm
Danilevskaya et al. (2003); Gutierrez-Marcos et al.
(2006);
Hermon et al. (2007); Haun and Springer (2008)
Danilevskaya et al. (2003); Gutie ́ rrez-Marcos et al.
(2006); Hermon et al. (2007)
Guo et al. (2003); Haun and Springer (2008)
Gutierrez-Marcos et al. (2003)
Gutie ́ rrez-Marcos et al. (2004)
Haun et al. (2007); Haun and Springer (2008)
Jahnke and Scholten (2009)
VIM5
YUC10
Paternal
Paternal
Parentalspecific
expression
Endosperm
Endosperm
Embryo
and
Endosperm
Endosperm
Endosperm
Kermicle (1970); Ludwig et al. (1989)
Chaudhuri & Messing (1994)
Lund et al. (1995a)
Lund et al. (1995b)
Zhang et al., (2011)
Zhang et al., (2011)