The role of APC/C in cell cycle dynamics, growth and development in cereal crops

Abstract

Cereal crops can be considered the basis of human civilization. Thus, it is not surprising that these crops are grown in larger quantities worldwide than any other food supply and provide more energy to humankind than any other provision. Additionally, attempts to harness biomass consumption continue to increase to meet human energy needs. The high pressures for energy will determine the demand for crop plants as resources for biofuel, heat, and electricity. Thus, the search for plant traits associated with genetic increases in yield is mandatory. In multicellular organisms, including plants, growth and development are driven by cell division. These processes require a sequence of intricated events that are carried out by various protein complexes and molecules that act punctually throughout the cycle. Temporal controlled degradation of key cell division proteins ensures a correct onset of the different cell cycle phases and exit from the cell division program. Considering the cell cycle, the Anaphase-Promoting Complex/Cyclosome (APC/C) is an important conserved multi-subunit ubiquitin ligase, marking targets for degradation by the 26S proteasome. Studies on plant APC/C subunits and activators, mainly in the model plant Arabidopsis, revealed that they play a pivotal role in several developmental processes during growth. However, little is known about the role of APC/C in cereal crops. Here, we discuss the current understanding of the APC/C controlling cereal crop development.

Full text

The role of APC/C in cell cycle
dynamics, growth and
development in cereal crops
Perla Novais de Oliveira
†
,Luı
´s Felipe Correa da Silva
†
and Nubia Barbosa Eloy*
Department of Biological Sciences, Escola Superior de Agricultura ‘Luiz de Queiroz’, University of
São Paulo, Piracicaba, Brazil
Cereal crops can be considered the basis of human civilization. Thus, it is not
surprising that these crops are grown in larger quantities worldwide than any other
food supply and provide more energy to humankind than any other provision.
Additionally, attempts to harness biomass consumption continue to increase to
meet human energy needs. The high pressures for energy will determine the
demand for crop plants as resources for biofuel, heat, and electricity. Thus, the
search for plant traits associated with genetic increases in yield is mandatory. In
multicellular organisms, including plants, growth and development are driven by
cell division. These processes require a sequence of intricated events that are
carried out by various protein complexes and molecules that act punctually
throughout the cycle. Temporal controlled degradation of key cell division
proteins ensures a correct onset of the different cell cycle phases and exit from
the cell division program. Considering the cell cycle, the Anaphase-Promoting
Complex/Cyclosome (APC/C) is an important conserved multi-subunit ubiquitin
ligase, marking targets for degradation by the 26S proteasome. Studies on plant
APC/C subunits and activators, mainly in the model plant Arabidopsis, revealed that
they play a pivotal role in several developmental processes during growth.
However, little is known about the role of APC/C in cereal crops. Here, we
discuss the current understanding of the APC/C controlling cereal
crop development.
KEYWORDS
cell cycle, cereal crops, plant development, anaphase promoting complex/
cyclosome, plant growth
Introduction
Monocotyledon crops, such as maize, rice, sorghum, wheat, and sugarcane, have a
huge impact on different aspects of human society, such as feed and food supply and
biofuel production, being the basis of the economy in several countries. Since the
implementation of monocultures in agriculture, humankind developed strategies to
Frontiers in Plant Science frontiersin.org01
OPEN ACCESS
EDITED BY
Aleksandra Skirycz,
Boyce Thompson Institute (BTI),
United States
REVIEWED BY
Alfredo Cruz-Ramirez,
National Polytechnic Institute of
Mexico (CINVESTAV), Mexico
Lixin Wan,
Moffitt Cancer Center, United States
*CORRESPONDENCE
Nubia Barbosa Eloy
nbeloy@usp.br
†
These authors contributed
equally to this work and share
first authorship
SPECIALTY SECTION
This article was submitted to
Plant Systems and Synthetic Biology,
a section of the journal
Frontiers in Plant Science
RECEIVED 06 July 2022
ACCEPTED 13 September 2022
PUBLISHED 29 September 2022
CITATION
Oliveira PN, da Silva LFC and Eloy NB
(2022) The role of APC/C in cell cycle
dynamics, growth and development in
cereal crops.
Front. Plant Sci. 13:987919.
doi: 10.3389/fpls.2022.987919
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© 2022 de Oliveira, da Silva and Eloy.
This is an open-access article
distributed under the terms of the
Creative Commons Attribution License
(CC BY). The use, distribution or
reproduction in other forums is
permitted, provided the original
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not comply with these terms.
TYPE Review
PUBLISHED 29 September 2022
DOI 10.3389/fpls.2022.987919

increase crop yield. Through the domestication of crop species,
farmers began to identify individuals with better traits among
others of the same species present in the plantation and started
to selectively propagate them for the next harvest. A large part of
the cultivated varieties grown nowadays was produced by this
technique, after the theoretical framework provided by Gregor
Mendel with the establishment of the heredity principles (Moose
and Mumm, 2008;Tester and Langridge, 2010). The following
years were marked by the definition of genetic inheritance laws
and advances in molecular biology (Kellenberger, 2004). These
events have paved the way for more detailed studies on key
individual components that affect specific plant characteristics,
such as life cycle, hormonal response, growth and development.
This technical-scientific revolution allowed the emergence of
new techniques, including genetically modified plants, to
increase agricultural productivity, highlighting the importance
of characterizing basic biological processes (Botstein, 2012).
Growth and development are two well-characterized
processes extensively studied in plants. The first refers to the
permanent and irreversible increase in volume and biomass of
the plant, which may or may not be accompanied by the addition
of new organs (Brukhin and Morozova, 2011). Development, in
turn, is responsible for the physical and morphological changes
in the plant body throughout its different stages of life (Drost
et al., 2017). Those two processes depend on energetic reactions
that generate specific cell patterns, which form specialized tissues
and shape the plant organs. Most plants exhibit an
indeterminate growth pattern, being able to grow even after
reaching reproductive maturity, an ability that differs from most
animals that achieve a maximum size at a specific age (Brukhin
and Morozova, 2011;Perianez-Rodriguez et al., 2014;Hariharan
et al., 2016). This indeterminate growth is due to the continuous
activity of meristematic tissues, allowing the generation of new
plant organs. The cells in these meristematic tissues divide and
generate new cells, some will remain as meristematic cells while
others will undergo differentiation and specialization, becoming
derivative cells. The specialized cells ensure that each organ will
play the function that is fated after cellular specialization, the
new cells continue to divide for some time to propagate the
differentiated region (Doerner, 2003;Stahl and Simon, 2010;
Hariharan et al., 2016;Kitagawa and Jackson, 2019;Umeda et al.,
2021). Thus, the development of an organism comprises a set of
processes that allow the transition from single cells to a complex
multicellular organism. Most animals, except for species that
undergo metamorphosis, complete their ontogenetic
development during embryogenesis, so the body plan of the
mature embryo is extremely similar to the adult but in smaller
proportions. Conversely, plants do not have an endpoint for
ontogenetic development, even after the short embryonic
development phase (Hariharan et al., 2016;Drost et al., 2017);.
Throughout embryogenesis, meristems originate only primary
structures, such as hypocotyl, cotyledons, and radicle (de Vries
and Weijers, 2017;Radoeva et al., 2019;Armenta-Medina
et al., 2020). Most of the true tissues and organs, including
flowers, roots, stems, and vascular systems, develop after seed
germination, in a post-embryonic developmental program,
which, like growth, occurs throughout the lifespan of the
plant. Moreover, organ development in plants occurs in a
sequentially way, by the addition of functional units called
phytomers (McMaster, 2005;Javelle et al., 2011;Perianez-
Rodriguez et al., 2014).
Cell division
In multicellular organisms, including plants, the processes of
growth and development are driven by cell division (Sablowski
and Carnier, 2014). The cell cycle brings together different
molecular and biochemical events that allow the emergence of
new cells (Inzeand De Veylder, 2006). Cell division is
characterized by four sequential phases, which temporally
separate the replication of genetic material from the
segregation of homologous chromosomes into two daughter
cells, making up the mitotic cell cycle. The DNA replication
(S) and mitotic entry (M) phases are separated by two gap (G)
phases. The G1 phase separates the end of mitosis and the
sequential S phase, while the G2 phase precedes the entry of
mitosis after the end of the S phase. Thus, cells in G2 have twice
the genetic material compared to cells in G1. G phases have
molecular mechanisms capable of verifying whether the previous
phase was completed correctly (Hunt et al., 2011;Kernan et al.,
2018;Matthews et al., 2022).The process of cell division requires
a sequence of intricated events that are carried out by a variety of
protein complexes and molecules that act punctually throughout
the cycle.
In all eukariotes, including plants, the cell cycle progression
relies on the activity of the CDKs (cyclin-dependent kinases), its
activity is essential to trigger the transition from the G
1
to S and
the G
2
to M phases. CDK regulation happens through
association with its regulatory subunits known as cyclins,
phosphorylation, dephosphorylation, interaction with
inhibitory proteins, and proteolysis (de Veylder et al., 2007).
However, the primary process which control the cell cycle
evolution are similar in all eukariotes, plants has unique
features controlling it. Usually they possess many more CYCs
and CDKs compared with yeast and animals. For example, in the
Arabidopsis genome there are 7 classes of Cyclins, comprising
about 50 genes, some of which have unknown functions. Among
them, the most studied are the A, B and D classes (Shimotohno
et al., 2021).The A-type cyclins are the regulators of S to M
transition, B-type cyclins control the G2 to M transition, while
D-type Cyclins are the G1-S trasition regulators, thus specific
interactions between different CYCs and CDKs are the key
feature to recognize the targets and promote regulation of the
differents cell cycle phases. About CDKs, the most known are the
CDKAs and CDKBs, being the latter only found in the plant
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kingdom, which are directly involved in cell cycle control (Polyn
et al., 2015).
To ensure a unidirectional progression of the cycle,
cellular degradation mechanisms break down specific proteins
that have phase-specificaction(Genschik et al., 2014). In
general, the ubiquitin-proteasome pathway is the main
destruction machinery. This multi-enzymatic pathway adds a
polyubiquitin tag on specific proteins, which will be recognized
and degraded by the 26S proteasome (Figure 2)(Xu and Peng,
2006;Marshall and Vierstra, 2019). The importance of the
ubiquitin-26S proteasome system (UPS) for plants can be
exemplified by the high number of genes involved in this
pathway in the Arabidopsis thaliana genome, covering
approximately 6% of the total genes (Hua and Vierstra, 2011).
The majority of those genes are responsible for the expression of
E3-ligases, which are the most diverse component of the
enzymatic cascade, necessary for the selective identification of
the substrate to be marked for proteolysis (Smalle and Vierstra,
2004;Marrocco et al., 2010;Serrano et al., 2018);. This unbalance
among the genes of the UPS enzymes can be illustrated by the
number of those genes in rice (Oryza sativa). While the rice
plant expresses 6 and 36 ubiquitin-activating enzyme (E1) and
ubiquitin-conjugating enzyme (E2), respectively, the number of
ubiquitin ligase enzyme (E3) genes exceeds 1100 (Al-Saharin
et al., 2022). According to their catalytic domain, the isoforms of
E3 ligases can be grouped into U-Box, HECT (homology to E6-
associated carboxyl terminus), and RING (really interesting new
gene). The U-box and HECT domains are mostly found in
monomeric enzymes, but only the second one is known to form
the E3-Ub intermediary (Wang et al., 2022). The RING-finger
domain is found as a monomeric domain in a single subunit
RING ubiquitin ligase and RBR (RING Between RING)
ubiquitin ligase, which targets ABA receptors for degradation
in different subcellular locations at root and leaves. Also, the
RING domain is found in muti-subunit enzymes, such as Cullin
RING Ligases (CRLs) domains (Fernandez et al., 2020;Wang
et al., 2022). The E3s that have the RING domain are the most
well characterized ligases in plants, remarkably the CRLs, once
these enzymes play important role in plant growth and
development (Chen and Hellmann, 2013;Serrano et al., 2018)
(Figure 1). The Skp1/Cullin/F-box (SCF)-related complex and
the Anaphase-Promoting Complex/Cyclosome (APC/C) are two
well-characterized E3-ligases of the CRLs type in plant cell cycle
control. It is already known that the SCF complex interacts with
the D-type cyclins, forwarding them to degradation, while APC/
C temporally removes the A- and B-type cyclins in the early-to-
mid mitosis progression (Inzeand De Veylder, 2006).
As the name suggests, the APC/C is a key enzyme during
anaphase initiation, allowing chromatid separation. Once
activated, the APC/C can selectively target securin for
degradation, which is an inhibitor of separase, an enzyme able
to break up the cohesin complex that holds the chromatids
together. The degradation of securin leads to separase activity
and, consequently, the segregation of chromatids, marking the
beginning of anaphase (Castro et al., 2005;de Lange et al., 2015;
Jonak et al., 2017;Kernan et al., 2018). Securins are widely found
in fungi and animals, but the presence of these proteins has not
been detected in plants. However, Cromer et al. (2019) have
reported two proteins, PATRONUS1 and PATRONUS2
(PANS1 and PANS2) in Arabidopsis, which would act
FIGURE 1
Ubiquitin-Proteasome System (UPS). The proteolysis in the UPS happens by sequential reactions catalyzed by three different enzymes. The
process starts with the activation of the ubiquitin by the ubiquitin-activating enzyme (E1), using an ATP molecule (1). Next, the activated
ubiquitin is transferred to the ubiquitin-conjugating enzyme (E2), which is responsible to interact with the ubiquitin ligase (E3) and conjugate the
ubiquitin to the substrate that is recognized by the E3 (2). Plant genomes encode hundreds of E3 ligases (the main E3 ligases found in plants are
represented in 3), that will target the different substrates, making them recognizable by the proteasome 26S, leading to the substrate
degradation (5).
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similarly to securin in plants. The authors observed that APC/C
is necessary for targeting PANS1 to trigger chromosome
separation. Also, they showed that both proteins are essential
to plant viability and can interact directly with SEPARASE
(Cromer et al., 2019). Chromosome separation is the main
reported function of the complex, but APC/C is also involved
in the exit from mitosis and in the G1 phase of the cell cycle
(Eytan et al., 2006;Alfieri et al., 2017). Since the discovery of the
complex, 25 years ago, intensive studies have uncovered
many aspects of APC/C regulation and its role in cell
metabolism, but we are still far from a full understanding of
this important cellular machinery, especially in monocot plants
(Yamano, 2019).
The differential expression of APC/C subunits in various
Arabidopsis tissues, even in completely differentiated cells, has
driven research interest in understanding what other roles the
complex can play in the organism (Lima et al., 2010;Eloy et al.,
2011). In this review, we bring some of these additional
functions performed by APC/C in different aspects of
plant development and growth in monocotyledons of
economic importance.
APC/C is a ubiquitin ligase with
multiple subunits
One of the most important mechanisms implicated in plant
cellular and developmental processes is the post-translational
regulation via ubiquitin-proteasome pathway/system (UPP/
UPS) (Sharma et al., 2016;Stone, 2019). The UPP/UPS
irreversibly conjugates ubiquitin moieties to the target
proteins, resulting in polyubiquitylated proteins that will be
recognized and degraded by the 26S proteasome, releasing the
free ubiquitin for recycling (Miricescu et al., 2018;Marshall and
Vierstra, 2019).
Protein ubiquitination is a multi-enzymatic cascade that
involves successive activity of the enzymes that compose the
UPS. The pathway starts with the E1-activating enzyme
activating and transferring one ubiquitin to an E2-conjugating
enzyme, in an ATP-dependent manner. Next, the E3 ubiquitin
ligase enzyme mediates the transfer of ubiquitin from E2 to a
lysine (Lys) residue into the target protein (Toma-Fukai and
Shimizu, 2021). This labeling process is repeated several times
because all seven Lys residues on the ubiquitin molecule are
ubiquitinated. The polyubiquitylation of target proteins
functions as a recognition motif for the large ATP-dependent
multicatalytic protease (26S), the proteasome, which will
subsequently degrade the polyubiquitinated proteins, using its
endopeptidase activity, into small peptides (Smalle and Vierstra,
2004;Vierstra, 2009)(Figure 2).
E3 ubiquitin ligases comprise a large and diverse family
among the three classes of enzymes involved in the
ubiquitination proteolytic pathway. APC/C, an important
conserved multi-subunit E3 ubiquitin ligase, is one of the most
complex molecular machines known able to catalyze
ubiquitination reactions. The complex mediates the
degradation of several eukaryotic key cell cycle proteins, such
as mitotic cyclins and securins (Petersen et al., 2000;Harper
et al., 2002;Capron et al, 2003;Buschhorn and Peters, 2006).
Besides its essentiality in cell cycle regulation, APC/C performs
specific functions during plant development. Through
functional characterization of their subunits, plant APC/C
proteins have been reported to play a role during cell
differentiation in shoot and root meristems (Blilou et al., 2002;
FIGURE 2
Relative expression profile of rice APC/C subunits and activators in different tissues. Expression analysis of genes from the APC/C subunits and
activators in shoots and roots (5-day old seedlings) and in leaf sheath and blade (120-day old plants) of rice. Expression levels are normalized to
root. Adapted from Lima et al., 2010.
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Lin et al., 2020;Schwedersky et al., 2021), plant growth (Saze and
Kakutani, 2007;Kuppusamy et al., 2009;Marrocco et al., 2009;
Rojas et al., 2009;Kumar et al., 2010;Eloy et al., 2011;Eloy et al.,
2012;de Freitas Lima et al., 2013), vascular development
(Marrocco et al., 2009), hormone regulation (Blilou et al.,
2002;Lin et al., 2020), tillering control (Lin et al., 2012;Xu
et al., 2012;Lin et al., 2020), female and male gametogenesis
(Capron et al., 2003;Kwee and Sundaresan, 2003;Eloy et al.,
2011;Zheng et al., 2011;Wang et al., 2012), and embryogenesis
(Perez-Perez et al., 2008;Awasthi et al., 2012;Wang et al., 2012;
Wang et al., 2013;Guo et al., 2016). In plants, APC/C is
composed of approximately 14 subunits, as seen in
Arabidopsis, maize, and sorghum, which are divided into at
least three main functional modules: a catalytic/substrate
recognition module, including the APC2, APC11, and APC10;
a structural module containing a tetratricopeptide repeat (TPR),
formed by APC3, APC6, APC7, and APC8 (D’Andrea and
Regan, 2003;Alfieri et al., 2017); and a scaffold module, to
which the catalytic and structural components are attached,
containing the APC1, APC4, and APC5 subunits (Thornton
and Toczyski, 2003;Thornton et al., 2006;Schreiber et al., 2011;
Chang et al., 2014;Chang et al., 2015;Eloy et al., 2015;Alfieri
et al., 2017). APC13 and APC15 are accessory subunits
responsible to promote the TPR association (Thornton et al.,
2006;Chang et al., 2014;Chang et al., 2015;Alfieri et al., 2017).
The CELL DIVISION CYCLE PROTEIN 26 (CDC26) subunit,
recently identified as part of the APC/C, contains an upstream
open reading frame (uORF) encoding a functional protein that
may control the translation of the main ORF (mORF) (Lorenzo-
Orts et al., 2019).
Although most of the studies about APC/C have been
carried out in budding yeasts (Saccharomyces cerevisiae), and
in plants, have been carried out in the model A. thaliana, little is
known about the complex in monocots. Homology-based
sequence analysis showed that almost every Saccharomyces
and Arabidopsis APC/C subunit are encoded by a single
counterpart gene in monocots, except for APC8 and APC11 in
rice, APC6,APC8,APC10,APC11, and APC15 in maize; and
APC11 in sorghum (Table 1). Furthermore, in maize and
sorghum, all APC/C subunits are present except for APC1
(Lima et al., 2010). In the rice genome, only a partial APC1
sequence is present, possibly due to misannotation (Lima et al.,
2010)(Table 1). These data suggest that monocots have all the
necessary components to assemble a functional and active
complex. Consequently, comparative genomic analyses can
provide valuable insights into the organization of the cell cycle
machinery and the evolution of these protein complexes,
indicating that the mechanisms that drive APC/C-mediated
proteolysis are conserved in organisms, including plants. Also,
according to Lima et al. (2010), expression patterns can provide
important clues for gene function under specific conditions. In
rice, for example, the expression of several APC/C subunit genes
has been investigated in roots and shoots of 5-day-old plants and
in the sheath and blade of mature leaves (Figure 3). As expected,
tissues with higher cell proliferation rates showed higher
expression levels of APC/C genes, however, with a pattern
varying from organ to organ (Lima et al., 2010). In general,
the mRNA levels of OsAPC1,OsAPC2,OsAPC4,OsAPC5,
OsAPC10,OsAPC11_2,OsCDC26, and OsAPC13 are reduced
in both sheath and blade compared to the total aerial part with 5
days old. Conversely, OsAPC11_2 and OsCDC27 mRNA levels
are reduced only in the sheath but not in the blade. Finally, there
is no reduction of OsAPC7 expression in both sheath and blade.
These results show that APC/C in monocots may have distinct
characteristics that can be important for its function in this
group, and the elucidation of these characteristics requires
additional investigation.
Two structurally related proteins act as co-activators of the
APC/C, ensuring the complex activity. The CELL DIVISION
CYCLE20 (CDC20) and the CDC20 HOMOLOG 1 (CDH1) are
found in all known eukaryotic genomes (Peters, 2006). The APC/
C co-activators are characterized by the WD-40 domain, tandem
repeats termed after a high frequency of tryptophan (W) and
aspartic acid (D) pairs, which represents the main site for protein
interactions (van Leuken et al., 2008). The WD-40 class proteins
are essential for providing catalytic activity and facilitating
substrate recognition in APC/C-dependent proteolysis (van
Leuken et al., 2008). The number of CDC20 copies varies
according to the species. In corn and sorghum, both genomes
hold two copies (CDC20.1 and CDC20.2), while the rice genome
contains three copies (CDC20.1,CDC20.2,andCDC20.3)
(Table 1). The plant CDH1 activators are known as CELL
CYCLE SWITCH52 (CCS52) proteins (Peters, 2002;Baker
et al., 2007;Breuer et al., 2012) and can be classified into A-
and B- types, known as CCS52A and CCS52B, respectively
(Cebolla et al., 1999;Tarayre et al., 2004;Kevei et al., 2011). The
rice genome has two CCS52 genes compared to three and two
genes in maize and sorghum, respectively (Table 1). The
overexpression of OsCCS52A in rice inhibits mitotic cell division
and induces endoreduplication, also known as endocycling or
endoreplication (detailed below), and cell elongation in fission
yeast (Su'udi et al., 2012b). In addition, T-DNA insertion in the
OsCCS52A resulted in rice plants with growth retardation
and smaller seeds showing endosperm defects during
endoreduplication. These phenotypes were attributed to
disruption of the endoreduplication cycle in the endosperm of
the mutant seeds, as evidenced by a reduction in nuclear and cell
size (Su'udi et al., 2012b). Tillering and Dwarf mutant 1 (tad1),
which is an ortholog of CCS52A (Xu et al., 2012), similarly caused
semi-dwarfism and leaf size decrease in rice. Furthermore, the rice
mutant line osccs52b exhibited a semi-dwarf and narrow kernel
phenotype due to a reduction in cell expansion (Su'udi et al.,
2012a). Microscopic analysis of mutant kernels showed that the
nuclear size and ploidy level were unaffected. Together, these
results suggest that OsCCS52B may be involved in cell expansion
regulation in rice endosperm (Su'udi et al., 2012a).
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TABLE 1 Genomic evolution of the Anaphase Promoting Complex/Cyclosome (APC/C).
A. thaliana O. sativa Z. mays S. bicolor S. cerevisiae
APC subunits Access number % identityO. sativa % identityZ. mays % identityS.bicolor % identityS.cerevisiae
APC1 At5g05560 Zm00001d037981 Sobic.009G104900 KAF4007119.1 49 50 27
APC2 At2g04660 Os04g40830 Zm00001d014685 Sobic.010G252700 EGA73963.1 63 64 64 22
APC3a At3g16320 Zm00001d042523 Sobic.003G388000 EEU08813.1 47 47 34
APC3b At2g20000 Os06g41750 Zm00001d042523 Sobic.003G388000 EEU08879.2 55 57 56 34
APC4 At4g21530 Os02g54490 Zm00001d052072 Sobic.004G322300 EEU08879.142 49 52 52 29
APC5 At1g06590 Os12g43120 Zm00001d040342 Sobic.003G123100 NP_014892.3 53 51 50 30
APC6a At1g78770 Os03g13370 Zm00001d028358 Sobic.001G443300 EEU08879.204 74 73 73 31
APC6b Zm00001d047979 72
APC7 At2g39090 Os05g05720 Zm00001d024858 Sobic.009G045000 –62 61 61
APC8a At3g48150 Os02g43920 Zm00001d017475 Sobic.004G295900 EEU08879.256 65 66 66 30
APC8b Os06g46540 Zm00001d042523 40 33
APC10a At2g18290 Os05g50360 Zm00001d009440 Sobic.009G217300 EEU08879.326 81 82 81 35
APC10b Zm00001d038881 77
APC11a At3g05870 Os03g19059 Zm00001d028837 Sobic.001G398600 EEU08879.348 89 89 90 40
APC11b Os07g22840 Zm00001d040164 Sobic.003G103400 88 37 37
APC13 At1g73177 Os07g44004 Grmzm6g522911 Sobic.002G387800 53
APC15a AT5g63135 Os02g38029 Zm00001d050944 Sobic.004G200000 52 55 55
APC15b Zm00001d017070 53
Activators
CDC20_1a At4g33260 Os09g06680 Zm00001d016034 Sobic.004G119700 EEU08879.448 71 70 72 46
CDC20_2 At4g33270 Os04g51110 Zm00001d000168 Sobic.004G270800 EEU08879.558 70 71 71 45
CDC20_3 At5g26900 Os02g47180 EEU08879.668 71 41
CDC20_4 At5g27080 EEU08879.779 44
CDC20_5 At5g27570 EEU08879.889 46
CDC20_6 At5g27945 EEU08879.1009 41
CCS52A1 At4g22910 Os03g03150 Zm00001d027430 Sobic.001G526300 EEU08879.1129 70 72 73 48
CCS52A1_2
CCS52A2 At4g11920 Zm00001d048472 EEU08879.1237 60 50
CCS52B At5g13840 Os01g74146 Zm00001d041957 Sobic.003G444100 EEU08879.1374 69 73 74 48
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Besides its activators, the APC/C is also controlled by
inhibitory proteins, which are known in Arabidopsis as
ULTRAVIOLET-B-INSENSITIVE4 (UVI4) and its homolog
OMISSION OF SECOND DIVISION 1 (OSD1)/GIGAS CELL
1(GIGAS)/UVI4-Like (Hase et al., 2006;d’Erfurth et al., 2009;
Van Leene et al., 2010;Heyman et al., 2011;Iwata et al., 2011).
The UVI4 and OSD1/GIGAS/UVI4-Like proteins are
considered negative regulators of the APC/C activity and have
a partially redundant action, since both can assemble to the
CDC20, CCS52A, and CCS52B co-activator subunits. Likewise,
the loss of UVI4 and OSD1/GIGAS/UVI4-Like negatively affects
the stability of the mitotic A-type cyclins (Heyman et al., 2011;
Iwata et al., 2011;Cromer et al., 2012). In the Poaceae family, for
example, an independent whole-genome duplication (Lloyd
et al., 2014) led to two subgroups of OSD1/GIGAS/UVI4-Like
genes and species of this family have, at least, one member of
each subgroup in their genome (d’Erfurth et al., 2009). The rice
genome contains two genes of OSD1/GIGAS/UVI4-Like
(Os02g37850 and Os04g39670), and it was shown that a single
mutation in the Os02g37850 was sufficient to give rise to the
meiotic defects observed in the mutant plants, resembling the
same phenotype observed in Arabidopsis osd1 mutant (Mieulet
et al., 2016). A single gene orthologous to OsOSD1 was identified
in barley and Brachypodium genomes, whereas the maize and
sorghum genomes harbor a tandem duplication of the OSD1
gene (Lloyd et al., 2014).
A
B
FIGURE 3
APC/C plays an essential role in regulating the development of cereal crops. (A) A model showing the APC/C
TE/TAD1
complex-mediated
degradation of MOC1. Tiller Enhance (TE)/Tillering and Dwarf 1 (TAD1) act as activators of the Anaphase Promoting Complex/Cyclosome (APC/
C) complex E3 ubiquitin ligase activity and targets MOC1 for degradation through interacting with the D-box by the ubiquitin–26S proteasome
pathway, and consequently represses tillering. (B) A proposed model for APC/C
TAD1-WL1-NAL1
module-mediated control of leaf width. TAD1
activates the APC/C E3 ubiquitin ligase activity and targets WIDE-LEAF 1 (WL1) for degradation. WL1 directly binds to the regulatory region of
NARROW LEAF 1 (NAL1) and recruits the corepressor TOPLESS-RELATED PROTEIN (TPR) to inhibit NAL1 expression by down-regulating the
level of histone acetylation of chromatin, and consequently, decreasing leaf width. Adapted from Lin et al., 2012 and Xu et al., 2012.
de Oliveira et al. 10.3389/fpls.2022.987919
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Another plant-specific regulator that directly interacts with
APC/C is SAMBA. In Arabidopsis, SAMBA has been identified
as a plant-specific regulator of the APC/C because its loss-of-
function results in increased cell proliferation during early
development, and biochemical analyses showed that the lack
of SAMBA stabilizes CYCA2;3 (Eloy et al., 2012). Moreover, the
endoreduplication rate of the samba mutant is higher, suggesting
that, despite the increased cell number, cells exit the division
cycle earlier.
In maize, CRISPR/Cas9 samba mutants also displayed
higher cell proliferation, due to increased cell division rate
with reduced cell size (Gong et al., 2022). However, despite the
seemingly conserved role of SAMBA in associating with APC/C
in maize (GRMZM2G157878), the phenotypic readout was
distinct in Arabidopsis and maize plants. The samba mutants
displayed dwarfism, erect upper leaves, reduced organ and tissue
growth, which most likely results from several inter-species
differences or a combination thereof (Gong et al., 2022).
Moreover, it is noteworthy that a visible difference in SAMBA
mRNA expression exists in Arabidopsis compared to maize. In
Arabidopsis, the SAMBA transcript was higher during
embryogenesis, decreased gradually when seedlings
germinated, and is restricted to the hypocotyl at 8 days after
stratification, while in maize, the expression of SAMBA is more
stable throughout the entire plant life cycle (Sekhon et al., 2011).
APC/C plays an essential role in
seed shape and size in cereal crops
Cereals are the main class of crops in the world supplying a
substantial portion of food and industrial raw materials to
mankind (Olsen, 2020). Mature cereal grains characteristically
contain three major structures: embryo, endosperm and/or
embryonic cotyledons, and seed coat. The endosperm accounts
for most of the seed’s volume. Its shape and size are highly
determined by cell size through growth and expansion
(Kobayashi, 2019), as well as by a large accumulation of
storage compounds, like carbohydrates, proteins, and/or lipids,
and water (Dante et al., 2014a;Hands et al., 2016). Grass
endosperm development has several distinct phases, which can
overlap considerably, such as early development, differentiation,
periods of mitosis and later endoreduplication, accumulation of
storage compounds, and maturation (Sabelli and Larkins, 2009).
The endoreduplication process has been extensively
described in monocot species (Sabelli and Larkins, 2009),
displaying a huge impact on their cell’s ploidy level (Dante
et al., 2014b). The endoreduplication cycle occurs during the
transition from the mitotic cell cycle to a modified cycle called
endocycle, during which DNA re-replication is stimulated
without subsequent chromosome segregation and cytokinesis
(Kobayashi, 2019). In this process, the chromatids are duplicated
exponentially, while the number of chromosomes remains
unchanged (Edgar and Orr-Weaver, 2001). Endoreduplication
is an integral part of plant development. This process is observed
in different cell types, however, it is more prominent in larger,
metabolically active, or highly specialized cells (Inze and De
Veylder, 2006;De Veylder et al., 2011) as the ones forming the
endosperm of Poaceae seeds (Sabelli and Larkins, 2009;Sabelli,
2012). The prevalence of endoreduplication in cereal grains
suggests that it might have been positively selected during
plant domestication and breeding (Nowicka et al., 2021).
During endoreduplication, as cells expand, metabolic products,
such as starch and storage proteins, are accumulated in the seed
endosperm (Sabelli et al., 2013). The peak of endoreduplication
events during the endosperm development occurs 15 days after
planting (DAP) (Sabelli and Larkins, 2009). Nowicka et al.
(2021), by using different barley cultivars, showed a natural
variation in the kinetics of this process. These cultivars have a
high degree of endoreduplication in endosperm during the
second half of the barley grain growth period, characterized by
the production of storage components (Dante et al., 2014a). The
major wave of endoreduplication started from ~6 DAP and
increased linearly to 20 DAP. In maize endosperm, this major
wave occurs at 12 to 14 DAP, while it peaked at 15–18 DAP
(Brian et al., 2001), and at 15~24 DAP in wheat (Sabelli and
Larkins, 2009).
Endoreduplication can influence cereal grain yield and
quality. For instance, the frequency of polyploidy and the
number of cells per endosperm are correlated with seed weight
in wheat (Brunori et al., 1993). The phenotypic and molecular
consequences of endoreduplication in endosperm remain
unclear and seem to be species dependent (Nowicka et al.,
2021). The onset of endoreplication occurs when CDK/Cyclin
complex is low or inactive (Lilly and Duronio, 2005;Inze and De
Veylder, 2006), which is often associated with the degradation of
mitotic cyclins by the APC/C and their activators (Cebolla et al.,
1999). In maize endosperm, induced S-phase CDK activity and
repressed M-phase CDK activity were proposed to trigger
endoreduplication cycles (Grafiand Larkins, 1995). Dante
et al. (2014b), when studying the expression patterns of some
cell cycle proteins like A-, B- and D-type cyclins, and A- and B-
type CDKs, as well as their kinase activity, demonstrated that
CYCA1-associated kinase activity was higher during the mitotic
stage of endosperm development. In contrast, CYCB1;3,
CYCB2;1, and CYCD5-associated kinase show higher activity
in the mitosis-to-endoreduplication transition. Furthermore, A-,
B-, and D-type cyclins were more resistant to proteasome-
dependent degradation in endoreduplicating endosperm
extracts compared to mitotic extracts. Taken together, these
results suggest that endoreduplication is associated with reduced
cyclin proteolysis through the ubiquitin-proteasome pathway
(Dante et al., 2014b).
CCS52 protein has also been reported to be involved in
endoreduplication in seeds (Larson-Rabin et al., 2009;Mathieu-
Rivet et al., 2010), however, collectively, OsCCS52A and
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OsCCS52B seem in part distinct from their dicotyledon orthologs.
The important cell cycle regulator gene CCS52A,byactivatingthe
APC/C, is responsible for the mitotic-endocycle transition and
modifications in its expression levels hamper the endosperm
development (Barroco et al., 2006;Su'udi et al., 2012a). To
investigate the functional role of the OsCCS52A during rice
development, the T-DNA-insertional mutagenesis approach was
used (Su'udi et al., 2012b). The osccs52a mutants exhibited smaller
seeds and poorly developed endosperm as a resultof decreased cell
and nucleus sizes. Thus, OsCCS52A was also confirmed to play an
important role during vegetative growth in rice plants, as well as
being involved in the endoreduplication process during
endosperm development. Moreover, reduced expression of the
OsCCS52B gene in rice plants negatively impacted seed and cell
size. However, no visible effect was observed during the
endoreduplication cycle (Su'udi et al., 2012a).
The APC/C regulation in
cereal crops
In addition to its essential role in the cell cycle progression,
the APC/C has also been reported to target different substrates in
non-proliferating cells, such as MONOCULM 1 (MOC1) gene,
identified as a key regulator of rice tillering and branching
control (Li et al., 2003). MOC1 encodes a transcriptional
regulator belonging to the GRAS (GAI, RGA, and SCR) family
(Pysh et al., 1999), and it is mainly expressed in the axillary buds,
promoting the initiation of the axillary buds and boosting their
outgrowth during the vegetative and reproductive stages. The
rice moc1 full knockout mutants are characterized by having a
single main culm without any tillers and reduced panicle
branches (Lin et al., 2012;Xu et al., 2012). In wheat, the
TaMOC1 gene, ortholog of rice MOC1, is a typical nuclear
protein with transcriptional activation motifs mainly involved
in spikelet development (Zhang et al., 2015). These observations
suggest that gene function is broadly conserved between species
but the phenotypic changes and developmental effects are
species-specific(Wang et al., 2018).
Moreover, two genes, Tillering and Dwarf 1 (TAD1) and
Tiller Enhance (TE), were identified by co-expression analysis
with MOC1 in the axil leaves, ensuring rice tillering and
branching control (Figures 3A,B). To perform the analysis,
the authors worked with rice plants from a mutant pool,
originated by self-crossing of a diploid plant from an
autotetraploid culture. TAD1 gene (Xu et al., 2012)was
identified and isolated from the tad1 mutant, which showed
an increased tiller number, reduced plant height, and twisted
leaves and panicles. Sequence analysis revealed that this
mutation was caused by a single base substitution at the
second exon of tad1 resulting in G to A change, which
produces a premature stop codon.
The te mutant (Lin et al., 2012), displayed a drastically
increased tiller number and a twisted flag leaf. Through in
vitro and in vivo interactions studies, the TAD1 and TE (Lin
et al., 2012;Xu et al., 2012) were classified as CCS52 orthologs in
rice. Sequence and phylogenetic analyses revealed that TAD1
and TE contain several conserved domains frequently found in
other Cdh1 homologs, including WD-40 repeats domain and
four motifs: CSM (Cdh1-specific motif), IR (APC binding
domain), CBM (mitotic RVL cyclin binding motif), and RVL
(mitotic cyclin binding motif). TAD1 and TE play an essential
role during MOC1 degradation via APC/C, which results in the
inhibition of tillering in rice. According to Xu et al. (2012),
TAD1-overexpressing plants showed a reduced tiller number,
which resembles the moc1 phenotype. Furthermore, TAD1
interacts with MOC1 by coimmunoprecipitation and
bimolecular fluorescence complementation (BiFC) assays,
forming a complex with OsAPC10 and acting as a co-activator
of APC/C to target MOC1 for degradation in a cell-cycle-
dependent manner. In the absence of TAD1 function, MOC1
fails to be recruited for the APC/C dependent degradation,
resulting in an accumulation of endogenous MOC1 proteins,
and thus increasing the tiller number in tad1 rice plants.TE is a
substrate-recognition and binding factor of the APC/C, forming
the APC/C
TE
complex and interacting with MOC1 and
OsCDC27 (Lin et al., 2012).
Rice te loss-of-function mutants exhibited increased and
reduced sensitivity to abscisic acid (ABA) and gibberellic acid
(GA) hormones, respectively (Lin et al., 2015). Both BiFC and
Co-immunoprecipitation (Co-IP) assays showed that TE
physically interacts with ABA receptors OsPYL (PYR1-LIKE)/
RCARs (REGULATORY COMPONENTS OF ABA
RECEPTORS) and promotes their degradation via proteasome
26S, repressing ABA signaling. Conversely, ABA inhibits APC/
C-
TE
activity by phosphorylating TE through activating the
Sucrose Non-Fermenting-1-Related Protein Kinase 2
(SnRK2s), which may interrupt the interaction of TE to its
substrates and subsequently stabilize OsPYL/RCARs. In
contrast, GA3 treatment reduced the accumulation of SnRK2
proteins and may promote APC/C
TE
-mediated degradation of
OsPYL/RCARs. Based on these data, it was proposed that
SnRK2-APC/C
TE
regulatory module represents a regulatory
hub underlying the antagonistic action of GA and ABA in
plants (Lin et al., 2015;Lin et al., 2020).
More newly, biochemical and genetic analyses revealed that
TAD1, WL1 (WIDE-LEAF 1), and NAL1 (NARROW LEAF 1)
function in a common pathway to control leaf width in rice (You
et al., 2022)(Figures 3A,B). WL1 gene was identified and
isolated from the wl1 mutant, which showed an increased leaf
width throughout the growing season. Sequence analysis showed
a single-nucleotide substitution from C to T was identified in the
annotated gene. In resume, WL1 protein was able to bind to the
regulatory region of NAL1 directly and then recruit the
de Oliveira et al. 10.3389/fpls.2022.987919
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corepressor TOPLESS-RELATED PROTEIN (TPR) to inhibit
NAL1 expression by regulating the level of histone acetylation of
chromatin. In wl1 rice plants, WL1 interacts with TAD1 and
activates the APC/C
TAD1
, which targets WL1 for degradation,
resulting in the decrease of endogenous WL1 proteins, and thus
increasing leaf width. Thus, these discoveries uncovered a new
mechanism underlying shoot branching and leaf width, and shed
light on the understanding of how the cell-cycle machinery
regulates plant architecture in monocots.
Perspectives
Results from our research group suggest that the proteins
forming the body of the APC, and others that interact with the
complex, play a key role during proliferation in plants, leading to
higher biomass (Rojas et al., 2009;Eloy et al., 2011;Eloy et al.,
2012). Moreover, several studies have identified numerous
proteins, such as hormone regulators, transcription factors,
cell-division regulators, and cell wall biosynthetic proteins, as
potential candidates for biomass enhancement (Cockcroft et al.,
2000;Biemelt et al., 2004;Matsumoto-Kitano et al., 2008;
Fornaleet al., 2012;Shen et al., 2012). Thus, engineered cereal
crops with increased biomass are an excellent resource to
overcome problems like adverse impacts of climate change,
food shortage, and fossil fuel dependency.
A central goal of crop deployment is to develop varieties that
meet our growing demands for better fitness and yield. Despite
the great contribution of conventional breeding to this field, it is
still necessary to develop new biotechnological tools such as
CRISPR to produce novel cereal cultivars exhibiting better traits
without compromising plant productivity.
The use of genetically modifiedorganismsorthe
identification of compounds with positive effects on plant
growth may increase the supply of biomass for different
purposes and accelerate classical breeding approaches to
ensure future crop productivity.
Author contributions
NE conceived the manuscript. PO and LS wrote and NE
revised and corrected the article. PO and LS prepared the figures.
All authors contributed to the article and approved the
submitted version.
Funding
This research was supported by the São Paulo Research
Foundation (FAPESP), NBE 2017/10333-8, PNO 2021/06611-8,
and LFCS 2021/03212-5.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the
authors and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed
or endorsed by the publisher.
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