全 文 ：Received: 2013–01–25　　　　Accepted: 2013–06–24
This study was supported by Research Fund of the Doctoral Program of Higher Education (200805720004) and Scientific Research Foundation for
Returned Scholars, Ministry of Education of China ([2009]1001).
HUANG Qiong-lin (1986 ~ ), PhD. Mainly study about innovative development and research of Chinese medicine, and is working in Guangdong
Medical College now. E-mail: perfecthql@163.com
* Corresponding author. E-mail: rayhe618@hotmail.com
热带亚热带植物学报　2013， 21(6)： 577 ~ 586
Journal of Tropical and Subtropical Botany
植物器官大小相关基因研究进展
黄琼林, 何瑞*, 詹若挺, 陈蔚文
(广州中医药大学中药资源科学与工程研究中心， 岭南中药资源教育部重点实验室， 广州 510006)
摘要： 器官大小是植物形态的一个重要特征，而且具有严格的种属特异性。植物器官大小虽然受到外在的环境因素(如光照、
营养等)的影响，但它是由内在特有的细胞数目和细胞大小决定的。许多基因能通过转录调节、蛋白合成、激素调节或松弛细胞
壁等途径作用于植物细胞繁殖和 / 或细胞扩张，它们的过表达或缺失表达能改变植物器官大小和加快植物生长。尽管如此，这
些基因是通过相对独立的途径起作用，在植物中难以阐明一个相对整合的器官大小基因调控网络，这也是亟待解决的问题。目
前，一些与器官大小相关的基因已经应用于农作物育种，并培育出显著增大的农作物品种，这也证实了利用器官大小基因进行
植物品种选育的可行性。因此，通过研究药用植物器官大小的基因，在分子水平上有目的地调控器官的大小和形态，是缓解当
前许多药用植物面临的资源紧缺、枯竭、濒危困境的可考虑途径之一。
关键词： 植物器官大小； 基因； 细胞增殖； 细胞扩张
doi: 10.3969/j.issn.1005–3395.2013.06.013
Research Progresses on Genes Involved in Regulation of Plant Organ Size
HUANG Qiong-lin, HE Rui*, ZHAN Ruo-ting, CHEN Wei-wen
(Research Center of Chinese Medicinal Resource Science and Engineering, Guangzhou University of Chinese Medicine, Key Laboratory of Chinese
Medicinal Resource from Lingnan, Ministry of Education, Guangzhou 51006, China)
Abstract: Organ size is an important morphological trail in plants, and shows significant differences among
species. Organ growth is influenced by environmental factors, such as light and nutrients; however, it is determined
by the intrinsic information of cell number and cell size. A large number of genes involved in regulation of cell
proliferation and/or cell expansion have been identified, and their up-regulated or down-regulated expression
change organ size and accelerate organ growth by means of transcription regulation, protein synthesis and
modification, hormonal regulation and cell-wall loosening, and so on. In spite of this, these genes act through
relative independent pathways, making it difficult to demonstrate an integrated regulation network in plants.
Further challenges will be the regulation pattern and molecular changes in different plant species. Several genes
participated in organ growth have been used in crop breeding, and produced significantly large crops. Similarly,
characterization of the genes involved in organ size control of Chinese herbs to artificially promote organ size and
morphology at the molecular level will contribute to overcome the shortage and endangerment of medicinal plants.
Key words: Plant organ size; Gene; Cell expansion; Cell proliferation
578 第21卷热带亚热带植物学报
Plants show various organ size from species
to species, even those closed related. Organ size
possesses rigorous species specificity in plant from
germination to mature, and is precisely controlled by
intrinsic mechanism of plant growth and development.
Leaf size occupies an important position in diverse
plant organ, especially affects the energy capture and
other physiological activities of plants[1–2]. Due to the
comprehensiveness and complexity determined by
internal and external factors, the regulation mechanism
that sets the final organ size is one of difficult aspects
in plants.
Although the final size of organs is influenced
by environmental factors, such as light and nutrients,
the developing organs were regulated by intrinsic
information about their final size. For example,
organ size shows amazing consistency among the
individuals with the same species, while significant
differences may exist among the species belonging
to the same genus. Both cell number and cell size are
related to setting of growth and development of plant
species-specific organ size, which are consequences
of coordination between cell proliferation and cell
expansion[3–6]. After cells leave the meristem, cell
division cycle activates and cells begin to expand.
Along with the water entering vacuole, the crosslink
among the polymers located at cell wall begins
loosening, which coupled with endoreduplication.
These processes promote cell size and increase cell
number, and the change from cell proliferation to cell
expansion or division determines cell number and
results in the final organ size[4,7]. A number of research
on regulating plant organ size were carried out to
trace the genes or related regulators participated in the
processes of cell proliferation and/or cell expansion,
and try to characterize their functions (Table 1).
Their gain or loss of function phenotypes revealed
promotive effects on final organ size. However,
many identified regulators were revealed working in
relatively independent pathways making it difficult to
develop an integrated regulation model of plant organ
size.
Here, we reviewed the reported genes involved
in organ size of plant in these years and divided them
into four main categories based on their functions.
Moreover, a perspective on the feasibility of utilizing
these genes in special plants, such as medicinal herbs
was provided.
Table 1 Genes involved in plant organ size
Gene Encoded protein
Expression
alteration
Possible mechanism Reference
Transcription related
ANT Transcription factor AP-2 OE Increase cell number [8 – 11]
ARF2 Transcription factor LOF Mediate gene expression in response to auxin and promote cell
division and expansion
[12 – 13]
ATAF2 NAC-domain transcription factor OE Enlarge cell significantly [14]
AtHB16 HDZip transcription factor LOF Promote cell expansion [15]
BIGPEATALp MADS-box transcription factor LOF Increase cell size and interfere with postmitotic cell expansion [16]
CIN TCP transcription factor LOF Promote cell division or cell proliferation [17]
GIF/AN3 Homolog of human SYT
transcription activator
OE Promote cell proliferation and increase cell number [18]
GRF1 Putative transcription factor OE Increase cell size and regulate cell expansion [19]
GRF2 Putative transcription factor OE Increase cell size and regulate cell expansion [19]
GRF5 Putative transcription factor OE Increase cell number and maintain cell size [18]
HRC1 At-hook transcription factor OE Increase both cell size and cell number [20]
JAGGED Putative transcription factor OE Promote cell proliferation [21 – 25]
JAW miRNA-319 (Target:
TCP2,3,4,10,24)
OE Reduce expression level of TCP transcription factors and
promote cell proliferation
[26 – 27]
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Gene Encoded protein
Expression
alteration
Possible mechanism Reference
NGATHA B3 transcription factor LOF Regulate both cell number and size via control over cell
cycling
[28]
OBP2 DOF transcription factor LOF Increase both cell number and cell size [29]
PPD Putative DNA-binding proteins LOF Prolong the period of dispersed meristematic cell proliferation [30]
RON2 WD-40 transcription repressor LOF Promote cell expansion and cell division [31]
Protein synthesis and modification
BIG BROTHER E3 ubiquitin ligase LOF Increase cell number [32]
DA1 Ubiquitin receptor LOF Increase cell number [33 – 34]
EBP1 ErbB3 binding protein OE Promote cell proliferation or cell expansion in different periods [35 – 38]
MED Mediator complex subunit LOF Promote both cell proliferation and cell expansion [39 – 40]
TOR Ser/Thr kinase OE Increase cell size; an enhancer of EBP1 [41]
UBP15 Ubiquitin-specific protease OE Control cell proliferation and increase cell number [42]
Hormonal regulation
Auxin
ABP1 Auxin binding protein OE Promote cell expansion or cell proliferation based on auxin
concentration
[42 – 47]
ARGOS Unknown protein OE Enlarge cell size and increase cell number [48 – 51]
AVP1 H+-pyrophosphatase OE Increase cell division [52 – 53]
Bassinosteroid
BEN1 Homologous to dihydroflavonol
4-reductase and anthocyanidin
reductase
LOF Regulate brassinosteroid levels and promote cell division [54]
BRI1 Brassinosteroid receptor kinase OE Promote cell elongation and differentiation [55]
EXO EXOPDIUM protein OE Increase transcript levels of the BR-up-regulated genes
involved in the mediation of BR-promoted growth and active
cell division
[56]
Gibberellin
GA20 oxidase GA20 oxidase OE Promote cell elongation [57 – 59]
Cytokinin
HOG1 Cytokinin-binding protein LOF Affect the expression of cytokinin primary response genes to
promote cell division
[60]
Cell-wall loosening agent
EXP3 Expansin OE Promote cell expansion and increase cell elongation [61]
EXP4 Expansin OE Increase cell size and mediate cell-wall loosening [62]
EXP10 Expansin OE Increase cell length significantly and cell number
inconspicuously
[63]
Others
ABAP1 Armadillo-BTB Arabidopsis Protein 1 LOF Increases cell division rates [64]
AGG3 G protein γ subunit OE Increasing the period of cell proliferation [65]
CNR Putative fw 2.2 ortholog LOF Increase cell number [66]
fw2.2 Similar to the human oncogene c-H-
ras p21
LOF Control carpel cell number [67]
KLU Cytochrome P450 monooxygenase OE Increase cell number and promote organ growth in a non-cell
autonomous manner
[68 – 69]
RPT2a Paralog molecule of the RPT2
subunit
LOF Promote cell expansion and increase DNA replication [70]
OE: Overexpression; LOF: Loss of function.
Continued
黄琼林等：植物器官大小相关基因研究进展
580 第21卷热带亚热带植物学报
1 Transcriptional regulation
It is no wonder that transcription factor participate
in organ growth and enhance organ size when ectopically
expressed. Intensive researches have been launched
to study how transcription factors AINTEGUMENTA
(ANT) and JAGGED (JAG) work. ANT is required
for flora organ development by regulating cell
division of integument and controls cell division and
organ size during the development of buds. Loss of
ANT function reduces the size of lateral organ by
decreased cell number. Conversely, ectopic expression
of 35S:ANT enhances ANT function and enlarges
embryos and buds attributed to increased cell number,
but the extrinsic shape of these organ is not altered. In
the fully differentiated organs, the cells overexpressed
ANT display neoplasia activity, and then give birth
to callus and form roots and buds occasionally.
Therefore, ANT regulates cell proliferation and
organ growth through maintaining meristematic
capability of cells during the organogenesis[8–11].
The recent studies also revealed that ANT and
related genes, AINTEGUMENTA-LIKE6 (AIL6) and
AINTEGUMENTA-LIKE7 (AIL7), functionally act
together in the meristem of young floral primordial,
carpel margin and shoot apical through auxin
transport[71–73].
JAGGED, encoding a putative transcription factor
with a single C2H2 zinc-finger domain, expresses
in all tissues and organs, and is a growth promoter
characterized by stronger tissue-expression specificity.
Loss of JAG function incompletely restricts the
development of lateral organ[21–23]. The correlation
between expressional threshold of JAG in the petal
and the redundant cell activities in cell cycle indicates
that JAG governs the growth by maintaining or
activating the activity of cell cycle. In addition, the
phenotypes of loss of JAG function are identical with
those overexpressed cyclin-dependent kinase inhibitor,
and the activities of cell cycle are suppressed, which
is another evidence revealing the function of JAG on
growth controlling[24–25]. Unlike other growth factors
(e.g. BIG BROTHER and ANT), JAG also promotes
morphogenesis of several lateral organs[8,22–23].
The growth-regulating-factor family members
(GRF1, GRF2, and GRF5) and their interacting protein
AN3/GIF1 have been confirmed as positive regulators
for organ size in Arabidopsis. Overexpression of all
these genes lead to increase of leaf size, however, the
result is caused by two processes. GRF1 and GRF2
enlarge leaf size contributed to cell expansion, while
GRF5/GIF1 increase the size by producing more
cells[18–19].
Gain-of-function of several transcription factors
show repressive effects on cell proliferation or cell
expansion, their expression levels were artificially
downregulated to promote organ size and yield.
Mutant of AUXIN RESPONSE FACTOR2 (ARF2)
significantly enhanced final seed size and weight by
promoting both cell proliferation and cell expansion[12].
Meaningfully, the expression level of ANT in this
mutant increased[13], speculating that these two genes
were possibly complementary to regulate cell processes.
Down-regulation members of TEOSINTE
BRANCHED1 / CYCLOIDEA / PROLIFERATION
CELL FACTOR1 (TCP) transcription factor family
remarkably enhanced leaf size and number through
overexpression of miRNA-319[26], and up-regulation
of miRNA-319 separately lead to similar results[27],
however, single mutants of TCP only exhibited slightly
enlarged leaves[26], indicating that microRNA probably
restricted the expression of TCP and participated in
regulation of organ size directly or indirectly.
Silent PPD increased leaf size by prolonging
the period of dispersed meristematic cell division[30].
Down-reguation expression of NGATHA also enlarged
leaves, flowers and cotyledons as well as stimulating
root growth[28].
2 Protein synthesis and modification
Except for transcription factor, protein regulation
at translation level plays a profound role in organ
growth. EBP1, a member of the PA2G4 family, was
identified as an epidermal growth factor receptor
(ErbB3)-binding protein. Expression of EBP1 is
第6期 581
ubiquitous in all tissues and cells[35–36] and rigidly
regulated in plants. The level is the highest in developing
organs, which closely related to genes involed in
ribosome biogenesis and function. During early peroid
of organogenesis, EBP1 promotes cell proliferaton,
influences cell-size threshold for division, and limits the
period of meristematic activities. In postmitotic cells,
it advances cell expansion. EBP1 is indispensable
for expression of cell cycle genes; CyclinD3;1,
ribonucleotide reductase 2 and the cyclin-dependent
kinase B1;1. The regulation of these genes by EBP1
is dose and auxin dependent, and upregulated EBP1
levels decreases the endogenous RBR1 protein, results
in the release of the E2F-dependent transcription
of these cell cycle genes and then, promotes cell
proliferation, which may be the mechanism that EBP1
set the final organ size[37]. EBP1 accelerates growth,
enlarges leaves and enhances cold tolerance by
enhancing ribosome biogenesis and the concomitant
translation of cold induced transcription factors and
downstream protective protein under cold stress in
transgenic Arabidopsis plants[38].
Target of rapamycin (TOR) encodes Ser/
Thr kinase and promotes organ growth by regulating
plenty of biological processes, such as translation of
ribosomal components. Overexpression of TOR also
promotes EBP1 level, which is validated in various
development stages[41]. The interrelation between
EBP1 and TOR suggests that EBP1 could be a target
of TOR and act downstream of TOR kinase on the
mRNA translation machinery.
Ubiquitination of proteins occupies a key part
in plant growth and exhibits promotive effect in
mutation. Encoding a putative ubiquitin receptor,
Arabidopsis DA1 (AtDA1, DA means “large” in
Chinese), as well as seven closely similar genes DA1-
related (AtDAR) controls final seed and organ size
by limiting the duration of cell proliferation in early
stage of organogenesis. da1-1, a mutant changing a
conserved amino acid at position 358 of AtDA1, has
a negative influence towards AtDA1 and AtDAR on
transgenic Arabidopsis and functionally independent
of ANT, AXR1 and ARF2. Overexpression of da1-1
significantly enlarges seed, flower, leaf, and seedling
size of wild-type Arabidopsis[33]. Interestingly, EOD1
(means enhancer of DA1) significantly enhances the seed
and organ size phenotype of da1-1, and is identified
as mutant of another plant growth repressor BIG
BROTHER[34], indicating that BIG BROTHER and
DA1 act in parallel pathways to control organ size.
Mediator complex subunit plays a key role in shade
avoidance and stress responses. Some members
of mediator complex subunit functionally reduce the
final organ size in plant. Overexpression of MED25
limits organ size with smaller and fewer cells, while
loss of MED25 function enlarges organ size with
large and inconspicuously increased number of cells,
implying that MED25 controls organ growth by
reducing both cell proliferation and cell expansion.
The mutants of MED25, called eod8-1 and MED25-2,
also enlarge floral organs and significantly enhance the
da1-1 phenotypes in Arabidopsis. MED25 functions
associating with DA1 to control final organ size by
restricted cell proliferation independent of MED25-
mediated phytochrome signaling and jasmonate[39].
MED8, another member of mediator complex subunit,
shows similar effect with MED25 by restricting
cell proliferation. However, MED8 is functionally
independent of MED25; they possibly transmit distinct
signals from different classes of activators to the RNA
polymerase II complex to initiate transcripts of their
respective downstream target genes involved in organ
size control[40].
3 Hormonal regulation
It is well known that hormones play a dominant
role in signaling transformation network, and together
with other signals, regulates cell processes, such as
cell division, elongation and differentiation in plant
cells. In particular, the roles of auxin, brassinosteroid,
gibberellins, and cytokinins in organ size have been
studied in plants.
黄琼林等：植物器官大小相关基因研究进展
582 第21卷热带亚热带植物学报
3.1 Auxin
ABP1 (Auxin binding protein 1) shows higher
expression in young meristem, such as terminal buds,
root tips and spires, than in other tissues and organs[43].
Overexpression of ABP1 enlarges mesophyll cell, while
antisense suppression of ABP1 dramatically reduced
cell expansion and inconspicuously influences on cell
division induced by auxin[44]. ABP1 is functionally
related to the concentration of auxin, it promotes cell
elongation with low level of auxin, while increases
cell division with high level of auxin[45]. Due to
promoting cell elongation with the TIR1 pathway and
cell division with RBR pathway in root and regulating
expression of the genes involved in auxin response,
ABP1 was considered as a key regulator for root growth
and auxin response in cell cycle[46–47].
A regulator of plant organ size highly induced by
auxin, auxin-regulated gene involved in organ
size (ARGOS), was identified from Arabidopsis.
Expression of sense or antisense ARGOS cDNA enlarges
or reduces aboveground organs in transgenic plants,
ascribing to alterations in cell number and the duration
of organ growth. Ectopic expression of ARGOS
prolongs both the neoplastic activity of leaf cells and
the expression of ANT and CycD3;1. Further studies
had showed that loss of function of ANT interrupts
the organ enlargement in the plants overexpressing
ARGOS, indicated that ARGOS functions upstream
of ANT to impact on meristematic ability of organ
cells. The induction of ARGOS by auxin is weaken
or totally suppressed in auxin-resistant1 (axr1) and
overexpression of ARGOS partially regains axr1
organ size. These discoveries suggested that ARGOS
conducts auxin signals downstream of axr1, regulates
cell proliferation and organ growth through ANT[48].
Expression of rice ARGOS gene in Arabidopsis enlarged
organ size by promoting both cell division and cell
expansion, however, the transgenic rice (Oryza
sativa) overexpressing OsARGOS did not reveal any
organ size change compared to the control, implying
that the mechanism of OsARGOS on controlling
organ size in rice is probably different from
in Arabidopsis[49]. Ectopic expression of a Chinese
cabbage (Brassica rapa) BrARGOS in Arabidopsis
increase the size of all tissues and organs, solely by
enhanced cell proliferation, but no contribution from
cell expansion[50]. Expression of ARGOS gene driven
by DMW promoters accelerates growth, significantly
increases leaf size and enlarges flowers in transgenic
tobacco (Nicotiana tabacum), and these phenotypic
traits are steadily shown in T2 transgenic plants, but
function of ARGOS in cell proliferation in tobacco is
far weaker than in Arabidopsis[51].
AVP, a gene encoding H+-pyrophosphate, has been
served as a controller of auxin transport. Upregulate
expression of AVP enlarged shoot and root size by
promoting cell proliferation[52–53].
3.2 Brassinosteroid
In generally, brassinosteroid (BR) enhances
shoots and roots growth by stimulating cell division.
EXO is a BR-up-regulated gene and enhances the
transcription of genes participated in the mediation
of BR-promoted growth. Overexpression of EXO
results in petiole elongation, leaf expansion and
root growth[56]. Another brassinosteroid regulator
BEN1 also elongates the Arabidopsis organs when
mutated[54]. Besides, BRI encodes a brassinosteroid-
sensitive receptor kinase and enlarges leaf petioles[55].
3.3 Gibberellins
Gibberellin (GA) plant hormones are indispensable
for cell expansion, stem elongation and flower
development. Gibberelin 20-oxidase (GA20ox)
is the key enzyme in the GA biosynthesis pathway
and catalyzes the oxidation and elimination of
carbon-20 to synthesize bioactive C-19 GAs[57–58].
Overexpression of GA 20-oxidase increases the level
of endogenous GAs and the transgenic Arabidopsis
exhibited elongated hypocotyls, enlarged leaves
and 25% taller than wild-type seedling[59]. In five
GA20ox genes from Arabidopsis named AtGA20ox1,
AtGA20ox5, GA20ox1, -2, and -3 were the dominant
paralogs in the regulation of organ growth, they
significantly promoted floral organ growth and
other development. AtGA20ox1 contributed more
第6期 583
in internode and filament elongation, AtGA20ox2
mainly acted in flowering time and silique length.
However, AtGA20ox3 was functionally independent
of AtGA20ox1 and AtGA20ox2 at most developmental
stages, including the floral transition[74–75].
3.4 Cytokinins
Cytokinins are a kind of plant hormones that
promote branching and leaf, shoot development. HOG1,
an encoded gene of cytokinin binding protein, shows
negative effect in plant stature by overexpression. In
the antisense suppression lines, Arabidopsis plants with
increased leaf size, profuse branching and more seed
production were obtained, because of the function of
HOG1 on promoting cell division[60].
4 Cell-loosen agents
Expansins are proteins involved in cell wall
extension and cell enlargement, and it maintains the
major structure of a cell when regulating the process.
As expected, ectopic expression of genes coding
expansins (EXP3, EXP4, EXP10, et al) under control
of 35S-CaMV promoter gives rise to the formation of
larger leaves in Arabidopsis[61–63].
The achievements highlighted here provide
new insight in controlling plant organ growth,
with however, little understanding on the regulation
pattern and molecular changes in different plant species.
Therefore, more studies should be carried out to
understand the connection across various pathways
regulating organ size and illustrate an integrated
regulation network in plants. In addition, how artificially
added factors (fertilizers, phytohormones, humidity, et
al) influence these growth pathways is also a challenge
in this field.
The discoveries on genes related to organ size
also motivate people to promote organ size of plants
by engineering the genes. Deepen and comprehensive
investigation on genes involved in organ size promote
the crops and herbs to meet the market demand, and
exhibits important implications in enhancing the
quality and quantity of crops and plants. By far, genes
involved in organ sizes have been applied in crop
plants, maize (Zea mays) and tomato (Lycopersicum
esculentum) with large size had been cultivated by
regulating these genes[66–67], but no similar researches
were found in medicinal plants. As special group
of plants, herbal medicine always plays key role in
human health, and the yield is important matter of
concern. In reality, many herbal medicines encounter
resource shortage and the resource obtained via existing
methods is incapable to meet clinic and market demands.
Characterization of the genes involved in organ size
control from Chinese herbs in order to artificially
regulate organ size and morphology at the molecular
level will contribute to overcome the shortage and
endangerment of medicinal plants. With the development
of Herb Genome Program including whole genome
sequencing of medicinal plants with endangerment
or/and those of great medical and pharmaceutical
importance[76], cloning and characterization of genes
involved in organ size of medicinal plants become
realistic. Plant genetic engineering, a series of technique
originated in molecular biology and used widely in
present researches, is well able to fulfill the steps in
the studies. In addition, lots of successful examples
in model plants and crops can be taken as guidance
for similar studies in medicinal plants. Enlarging the
size of leaves or whole plants is one of considerable
and feasible ways to raise yield, especially on the
condition that the active ingredients of quite a few herbal
medicine remains unclear. Undoubtedly, attentions
should be drawn to some critical questions in the area.
Such as, whether there is any change of total chemical
components and pharmacological effects occur in
transgenic medicinal plants, how transformation of alien
genes influences the synthesis pathways of secondary
metabolites in medicinal plants, etc. Further and
extensive studies should be carried out to enhance final
organ size with the genes and to understand how they
influence growth and development of medicinal plants.
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