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First published online July 31, 2009; 10.1104/pp.109.141838 Plant Physiology 151:655-668 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
The Arabidopsis GRF-INTERACTING FACTOR Gene Family Performs an Overlapping Function in Determining Organ Size as Well as Multiple Developmental Properties1,[C],[W],[OA]Department of Biology (B.H.L., J.-H.P., J.H.K.) and School of Applied Bioscience (S.L.), Kyungpook National University, Daegu 702–701, Korea; Department of Forestry, Michigan State University, East Lansing, Michigan 48824 (J.-H.K.); and Department of Industrial Plant Science and Technology, Chungbuk National University, Cheongju 361–763, Korea (Y.L.)
Previously, the GRF-INTERACTING FACTOR1 (GIF1)/ANGUSTIFOLIA3 (AN3) transcription coactivator gene, a member of a small gene family comprising three genes, was characterized as a positive regulator of cell proliferation in lateral organs, such as leaves and flowers, of Arabidopsis (Arabidopsis thaliana). As yet, it remains unclear how GIF1/AN3 affects the cell proliferation process. In this study, we demonstrate that the other members of the GIF gene family, GIF2 and GIF3, are also required for cell proliferation and lateral organ growth, as gif1, gif2, and gif3 mutations cause a synergistic reduction in cell numbers, leading to small lateral organs. Furthermore, GIF1, GIF2, and GIF3 overexpression complemented a cell proliferation defect of the gif1 mutant and significantly increased lateral organ growth of wild-type plants as well, indicating that members of the GIF gene family are functionally redundant. Kinematic analysis on leaf growth revealed that the gif triple mutant as well as other strong gif mutants developed leaf primordia with fewer cells, which was due to the low rate of cell proliferation, eventually resulting in earlier exit from the proliferative phase of organ growth. The low proliferative activity of primordial leaves was accompanied by decreased expression of cell cycle-regulating genes, indicating that GIF genes may act upstream of cell cycle regulators. Analysis of gif double and triple mutants clarified a previously undescribed role of the GIF gene family: gif mutants had small vegetative shoot apical meristems, which was correlated with the development of small leaf primordia. gif triple mutants also displayed defective structures of floral organs. Taken together, our results suggest that the GIF gene family plays important roles in the control of cell proliferation via cell cycle regulation and in other developmental properties that are associated with shoot apical meristem function.
The size and shape of lateral organs, such as leaves and flowers, are under the control of developmental genetic programs exhibiting species-specific characteristics. In general, lateral organs from plant species of different size differ in cell number rather than cell size, as exemplified in the case where big petals of Brassica napus have the same size of cells as small petals of Arabidopsis (Arabidopsis thaliana) do (Mizukami and Fischer, 2000  ; Mizukami, 2001). Thus, cell number is a primary determinant of organ size of a species, although concomitant and/or subsequent cell expansion amplifies and modifies the effect of cell number, contributing to the final size and shape of lateral organs (Tsukaya, 2005; Cho et al., 2007).
Many genetic approaches have been employed to understand the control of cell proliferation and its role in organogenesis, and these have identified a number of genes that play important roles in the process. Some of these genes, such as AINTEGUMENTA (ANT), KLUH (KLU), and STRUWWELPETER (SWP), play positive roles (i.e. their loss-of-function mutants developed small lateral organs due to a reduction in cell numbers; Mizukami and Fischer, 2000
We have previously uncovered a novel class of transcriptional factors, GROWTH-REGULATING FACTOR (GRF), comprising nine members in Arabidopsis (Kim et al., 2003 Meanwhile, it still remains to be elucidated by what mechanism the GIF1/AN3 gene regulates cell proliferation and what biological roles the other two members, GIF2 and GIF3, play in Arabidopsis growth and development. In this article, we show that all of the GIF genes act as positive regulators of cell proliferation of lateral organs in a functionally redundant manner. Our results indicate that GIF genes may affect the duration of cell proliferation by modulating the expression level of cell cycle regulators. We also present experimental evidence that GIF genes are required for other developmental processes, such as plastochron and flower structure.
In Silico Expression Profiles of GIF Genes and Isolation of T-DNA Insertional Mutants
Using RNA gel-blot analysis, we have previously shown that the GIF family genes share an overlapping expression pattern and that GIF1/AN3 mRNAs are most abundant compared with GIF2 and GIF3 (Kim and Kende, 2004
A phylogenetic analysis suggested that GIF2 and GIF3 genes might result from a duplication event of a common ancestral gene after diversification from GIF1/AN3 (Kim and Kende, 2004
Growth and Developmental Phenotypes of Lateral Organs
As described previously (Kim and Kende, 2004
Unexpectedly, we found that the triple mutant displayed aberrant structures of floral organs, including split carpels and reduction in numbers of petals and anthers, while the wild type, single mutants, and gif2/3 showed normal floral organization and organ numbers; gif1/2 and gif1/3 double mutants displayed such floral defects but only in the terminal two flowers (Fig. 2C, last column; details will be described elsewhere). This observation confirmed the contribution of single mutations once more. In addition, gif1/2 and gif1/2/3 mutants were completely sterile, whereas other mutants set seeds, the number of which was variable depending on their phenotypic severity (Table I). Because of their infertility, gif1/2 and gif1/2/3 mutant lines were maintained in the heterozygous gif1 mutation with other homozygous ones. The sterility problem of gif1/2 seemed to stem from an abnormal functionality of female reproductive organs rather than from pollen. In other words, the gif1/2 double mutant produced pollen that was fully functional on wild-type carpels, producing as many seeds as wild-type pollen did, whereas wild-type pollen did not produce even a single seed on gif1/2 carpels (Supplemental Table S1). The gif1/2/3 triple mutant, besides the structural abnormality of flower organs, produced no pollen at all. These results indicate that GIF genes are also required for the maintenance of structural integrity and reproductive function of flower organs.
We determined cell numbers and sizes of lateral organs by observing subepidermal cells under Nomarski optics. Numbers of adaxial palisade cells in the first two mature leaves of gif1/2/3 were only 27% in the longitudinal axis and 15% in the maximum-width axis over wild-type plants (Fig. 3A, middle). The total number of palisade cells of the triple mutant, calculated by dividing leaf area by cell area, was only 4% of the wild type. The number of trichomes on the first two leaves of gif1/2/3 was also reduced to 8% of wild-type plants, which is indicative of a great reduction in the number of epidermal cells as well (Fig. 3A, right). Reduction in those cell numbers of other single and double mutants corresponded to changes in the organ-level dimensional parameters (Fig. 3A, compare left and middle panels). To the contrary, cell area of the triple mutant increased by 2.6-fold over the wild type (Figs. 2D and 3A), which probably resulted from a "compensatory" effect due to the drastic reduction in cell number (Tsukaya, 2003 ). It should be noted, however, that the compensatory increase in cell area was only partially able to make up for the reduction in leaf size, and there was no change in cell shape (Fig. 2). The gif1/2 double mutant exerted its compensatory effect to an extent comparable with the triple mutant, and that of the gif1 single and gif1/3 double mutants was also apparent. Other single and double mutants, however, did not show a significant change in cell area. These results indicate that the compensation occurs in direct proportion to the change in cell numbers. This is also true for cotyledons and flowers: more gif mutations resulted in smaller organs with fewer but bigger cells (Fig. 3, B and C). Taken together, our data indicate that GIF2 and GIF3 as well as GIF1 are involved in the positive regulation of cell proliferation of lateral organs in a functionally redundant manner.
To obtain more information about the effect of gif mutations on cell proliferation, we performed kinematic analysis on leaf growth. The first pairs of leaves were harvested at the indicated days from 4-d-old seedlings. Because gif1/2 double and gif1/2/3 triple homozygous mutants showed distinctively small and narrow cotyledons (Fig. 2B), we were able to differentiate homozygous individuals in the segregating populations of gif1/+ gif2/gif2 and gif1/+ gif2/gif2 gif3/gif3 genotypes. Leaf area continued to increase over time: slow during the early stage, then at an accelerated rate, and lastly, leaf expansion slowed toward the final size of mature leaves (Fig. 4A , left). Leaf expansion of wild-type plants was almost completed at day 20, whereas that of the gif1 single mutant and the gif1-harboring double mutants ceased at 17 and 13 d, respectively. The gif1/2/3 triple mutant showed only a minute leaf expansion during the whole growth period. Plotted on a natural log scale in a magnified version, the leaf area data from days 4 through 7 revealed that gif1/2/3 leaves were markedly smaller, by 5.5-fold, than wild-type leaves already at day 6 and afterward (Fig. 4A, right). A clear distinction between the gif1/2 double mutant and the wild type was also recognized at day 7. Intriguingly, however, leaf area of the gif1 single mutant was not smaller than that of the wild type in those early days; only later did it become smaller, eventually reaching half the size of wild-type leaves. This is consistent with what we have observed during plant growth: note the similar size of the first two leaves of the wild type and the gif1 single mutant even at day 8 in Figure 2B. We attribute this apparent discrepancy in size of young and mature gif1 leaves to the strong plastochronic properties of the gif1 mutant (see below).
To compare cell proliferation patterns of the wild type and mutants during leaf growth, we determined the number of adaxial palisade cells in a line along with a maximum-width axis of the first two leaves, and the resulting kinematic graph clearly showed that cell proliferation ceased at day 11 in the wild type but at day 7 in the strong mutants harboring gif1 (i.e. gif1, gif1/2, gif1/3, and gif1/2/3; Fig. 4B, left). Previously, Ferjani et al. (2007) also observed that an3-4, another mutant allele of GIF1, exhibited early cessation of the cell proliferation phase in the leaf-length axis. Moreover, leaves of gif1/2 double and gif1/2/3 triple mutants had only about half the cells of wild-type leaves already at days 6 and 4, respectively (Fig. 4B, right). Intriguingly again, however, gif1 leaves at the early stage between days 4 and 6 had more cells than wild-type leaves, at least partially explaining the reason why the leaf size of the gif1 mutant was similar to that of the wild type in those early days (Fig. 4B). This tendency in gif1 was consistently observed in an3-4 (Ferjani et al., 2007). Calculation of cell proliferation rate (changes in cell numbers between consecutive days divided by the cell number of the previous day) showed that cell proliferation in leaf was most active during the interval between days 5 and 7, but maximum proliferation activity of most gif mutants was remarkably or slightly lower than that of the wild type; especially, that of triple mutants was close to zero (Fig. 4C). Furthermore, almost no cell proliferation activity of the strong mutant lines was detected around day 8 and thereafter, whereas wild-type activity remained at a substantial level until day 10. These data indicate that the gif mutations exert synergistic effects on both the rate and duration of cell proliferation. Leaf cell expansion of the wild type and all of the gif mutants increased in a sigmoidal pattern throughout growth (Fig. 4D, left). The compensatory enhancement of cell expansion in the gif triple mutant became prominent from day 6, although it was not possible to make a clear distinction between the wild type and mutants before that day (Fig. 4D, right). It should be noted, however, that the enhanced cell expansion was not sufficient to mask the effect of the reduced cell proliferation on determining leaf size: already at day 6 and thereafter, leaf size of the triple mutant was at least five times smaller than that of the wild type (Fig. 4A).
The low rate of cell proliferation of gif mutants prompted us to examine the expression of cell cycle-regulating genes. Total RNA was isolated from the first two leaves of 6-d-old wild-type and gif1/2/3 triple mutant plants, in which their cell proliferation occurred at a maximum rate, and subjected to RT-PCR. The transcript levels of two cyclin genes, CycB1;1 and CycD3;1, as well as a cyclin-dependent kinase gene, Cdc2b, were significantly reduced in the triple mutant (Fig. 5
). Both CycB1;1 and Cdc2b are involved in the G2/M transition (Mironov et al., 1999
Mutant Phenotypes in the SAM Tissues
Since cells in the SAM continue to be recruited into developing leaf primordia (Telfer and Poethig, 1994
Plastochronic Properties of gif Mutants Apart from the cell proliferation phenotype, we noticed that gif mutations seemed to accelerate various developmental processes. To estimate the developmental acceleration, we measured the time when leaves reach 1 mm in length with a stereoscope in long-day conditions. The first two leaves of the gif1 mutant attained that length at day 7.8, which was 0.8 d earlier than the wild type (Table I). The third and fourth gif1 leaves were much earlier than the wild-type leaves, by 1.7 and 2.2 d, respectively. The difference between the wild type and gif1 was profound in the short-day conditions (i.e. gif1 leaves attained the length more than 3 d earlier compared with the corresponding wild-type leaves, clearly indicating that the gif1 mutation accelerated the early developmental pace). The time intervals at which successive leaves reached that length (plastochron) were also significantly shortened in the gif1 mutant compared with the wild type: for instance, it took 3.9 and 4.6 d in the respective photoperiods for the wild-type third leaf to attain 1 mm of length after its first two leaves did so, but it took 3.0 and 3.9 d for the gif1 third leaf under the corresponding conditions. However, the final numbers of wild-type and gif1 leaves were not significantly different from each other, and neither was germination time (data not shown). Taken together, these results clearly indicate that the gif1 mutant displays short plastochronic length at the early developmental stage as well as the hasty emergence of the first two leaves; furthermore, they explain why the gif1 single mutant has more cells in the primordial leaves at the early stage than wild-type primordium does, despite its lower cell proliferation activity, as mentioned above. In contrast, the time when the double mutants harboring the gif1 mutation, gif1/2 and gif1/3, attained 1-mm-long leaves was slightly delayed or similar, compared with their parental gif1 single mutant in both photoperiodic regimens, although they did so earlier than the wild type. Especially, the first two leaves of the gif1/2/3 triple mutant were more delayed than even the wild-type plant, by 1.9 and 0.2 d (compare the numbers in brackets in Table I for both photoperiodic regimens). It is important to realize, however, that this does not necessarily mean that no or antagonistic plastochronic synergism exists between those mutations. Rather, this observation means that leaves of gif double and triple mutants, unlike gif1 leaves, were so short that the time for the attainment of a 1-mm-long leaf could not be an appropriate parameter for plastochronic comparison with the wild type or gif1. In fact, the gif1/2/3 plastochron between the first two and third leaves was exceptionally shorter than that of gif1 (compare the numbers in parentheses in Table I), and synergistic acceleration of other developmental processes was evident: the gif1 mutant bolted 2 d earlier than the wild type did, and addition of the gif2 and gif3 mutations gradually shortened the bolting time, resulting in the gif triple mutant bolting 8 d earlier than the wild type (Table I). It is interesting that, in spite of their minute effect on leaf size, gif2/3 and gif1/3 double mutations shortened the bolting time a little more than the gif1/2 double mutation did. We also found that mutants containing the gif1 mutation developed more axillary branches, as shown in Figure 7A , in which all of the primary shoots and leaves, except two cotyledons, were removed to expose axillary branches at day 30. The triple mutant showed a long primary branch (Fig. 7A, far right). During the vegetative stage or just before bolting, only the gif triple mutant was able to develop primary branches from cotyledons and rosette leaves (i.e. nine out of 10 gif1/2/3 mutants showed a pair of rapidly growing axillary leaves from both cotyledons and the first two rosette leaves at day 17.0 ± 0.7 and 19.1 ± 0.7, respectively, whereas none of the other mutants as well as the wild type did so during the same period, although gif1/2 double mutants occasionally did). The triple mutant produced about five more primary axillary branches from rosette leaves and even cotyledons than the wild type, and other mutants harboring gif1 mutations showed intermediate numbers (Fig. 7C). To the contrary, there was no significant difference in numbers of primary branches derived from cauline leaf axils (Fig. 7D). These data indicate that the loss of GIF genes accelerates various developmental processes, including leaf plastochron.
Finally, the gif triple mutant developed short inflorescence stems, although other mutant plants containing the gif1 mutation tend to have a little longer stem than the wild type (Table I), suggesting that all three GIF genes are necessary for normal growth of the inflorescence stem.
To test whether or not GIF2 and GIF3 genes will be able to complement the gif1 phenotype, gif1 mutant plants were transformed with GIF1, GIF2, and GIF3 cDNAs under the control of the cauliflower mosaic virus 35S promoter. Dozens of T1 generation plants were obtained for each construct, and most of them showed a wild-type-like phenotype (Fig. 8A ; data not shown). Quantification data revealed that leaf dimension parameters of gif1 plants overexpressing each construct were very close to those of the wild type (Fig. 8B). Leaf indices were also recovered to the wild-type value, displaying leaves with round shape rather than the narrow one of the gif1 mutant. All of these dimensional changes corresponded exactly to those in cell numbers (Fig. 8C). We also established overexpressor lines whose gif1 mutation was segregated out after crossing the complementation lines to wild-type plants and found that overexpression of each gene in the wild-type genetic background increased both leaf area and cell numbers up to 14% (Fig. 8, D and E). These results indicate that the gain-of-function effects of GIFs on lateral organ growth are highly similar to each other, stimulating cell proliferation and organ growth.
In this study, we presented, to our knowledge, the first loss- and gain-of-function evidence that GIF2 and GIF3 acted as positive regulators for lateral organ growth, as did GIF1. We were also able to determine contributions of individual GIF genes to the biological function through phenotypic analyses of a series of multiple gif mutants. gif triple mutants also revealed novel phenotypes that are relevant to functional activities of the shoot apical meristem, such as plastochronic and axillary branching properties, as well as reproductive organ function and structure.
We demonstrated that GIF genes have an overlapping expression pattern in many different tissues and that gif mutations act synergistically to induce dramatic reductions in cell numbers of lateral organs, such as leaves and flowers as well as cotyledons (Figs. 1–3
Overexpression of GIF and GRF genes stimulated organ growth but to a limited extent (Fig. 8; Kim et al., 2003
Judged from the abnormal structure of flower organs, as mentioned briefly, and the plastochronic phenotype (Figs. 2 and 7; Table I), it seems that GIF genes play an important role in regulating other aspects of shoot development. It remains unknown whether those phenotypes are in any causal relationship to the cell proliferation process. With respect to the pleiotropic phenotype of gif mutants, it is interesting that the human homolog of the GIF proteins, SYT transcription coactivators, also show diverse biological roles in human cells via interaction with a plethora of proteins (Eid et al., 2000
It is conceivable that cell numbers in a plant organ could be determined in several different ways: (1) the frequency of cell proliferation; (2) the duration of cell proliferation; and (3) the number of cells in the primordial cell pool (Autran et al., 2002
The fact that the gif triple mutant produces leaf primordia with fewer cells raises the following possibility: besides low frequency of cell proliferation (Fig. 4), the leaf primordium of gif mutants may serve as a poor reservoir of progenitor cells available for further cell division. That, in turn, would lead to earlier exhaustion of meristematic cells, resulting in the earlier cessation and, thus, the short duration of cell proliferation. Autran et al. (2002)
One of the key functions of the SAM is to form lateral organs, such as leaves and flowers, from its peripheral zone. It has been proposed that the growth of young developing primordium is preceded by active mitosis in a large part of the SAM L1 layer (Laufs et al., 1998b
Meanwhile, it has been well documented that, in general, plastochron length and SAM size are inversely correlated in Arabidopsis. The cytokinin mutants and transgenic plants mentioned above have much smaller SAM and fewer leaves compared with the wild type, which is indicative of a longer plastochron (Werner et al., 2001
Plant Material
The Arabidopsis (Arabidopsis thaliana) seeds were sown on wet soil (Mix5; Sunshine), stratified at 4°C for 3 d, and transferred to a growth room at 23°C under a photoperiod of 16 h of light/8 h of darkness, which was marked as day 0 throughout the experiments. For measurement of leaf plastochron, plants were grown under the short-day conditions of 8 h of light/16 h of darkness. Wild-type plants and all of the T-DNA insertional mutants were in the Columbia ecotype. gif1 (SALK_150407; Kim and Kende, 2004
Homozygous mutant plants were selected by PCR-assisted genotyping. Primers for amplification of wild-type GIF genes and T-DNAs are described in Supplemental Table S2. DNA fragments amplified with the gene-specific and left-border primers were sequenced to confirm the T-DNA insertion site. The double homozygous lines, gif1 gif2, gif2 gif3, and gif1 gif3, were established through crosses between each homozygous line. The gif1 gif2 double mutant was maintained in the gif1/+ gif2/gif2 genotype, as it was female sterile, although it produced fertile pollen. The gif1 gif2 gif3 triple mutant was obtained as the F2 progeny of the cross between gif1 gif2 (male) and gif2 gif3 (female) and maintained in gif1/+ gif2/gif2 gif3/gif3.
GIF1, GIF2, and GIF3 cDNAs were amplified by PCR using primer pairs containing the Gateway partial recombination site at the 5' end, attB1 or attB2 (for primer sequence information, see Supplemental Table S2). The amplified DNA fragments were used as template for a second round of PCR with adaptor primers. The final cDNA fragments were inserted into the entry vector pDONR221 by the BP recombinant reaction, according to the manufacturer's protocol (Invitrogen). The resulting plasmids were used in the LR reaction with the destination vector pB2GW7,0 (http://www.psb.ugent.be/gateway) to produce GIF overexpression constructs driven by the cauliflower mosaic virus 35S promoter. The recombinant binary plasmids were introduced into gif1 mutant plants by Agrobacterium tumefaciens-mediated transformation (Clough and Bent, 1998
For determination of GIF mRNA content in T-DNA insertional mutants, total RNAs were extracted with TRIzol reagent (Invitrogen) from 15-d-old wild-type and mutant plants, treated with DNase I (DNA-free; Ambion), and subjected to RT (SuperScript II; Invitrogen). The resulting cDNAs were used for PCR amplification, the conditions for which were as follows: denaturation at 95°C for 2 min, followed by 34 cycles of 95°C for 15 s, 52°C for 30 s, and 72°C for 1 min (for primer sequence information, see Supplemental Table S2). For determination of transcript levels of cell-cycling regulators, cDNAs were prepared from the 6-d-old first two leaves as mentioned above, serially diluted to the indicated factors, and used for amplification. PCR conditions were as follows: denaturation at 95°C for 2 min, followed by 29 cycles of 95°C for 15 s, 52°C for 30 s, and 72°C for 1 min (for primer sequence information, see Supplemental Table S2).
The microarray data of the AtGenExpress expression atlas were retrieved from The Arabidopsis Information Resource (Schmid et al., 2005
Digital images of detached leaves, cotyledons, and petals were acquired using a scanner. Area, length, and width of leaves, cotyledons, and mature petals as well as petioles were determined with the image-analyzing program SCIONIMAGE (Scion). For kinematic analysis of leaf area, young leaves up to day 9 were detached and mounted on slide glass for light-microscopic image analysis.
Leaf, cotyledon, and petal tissues were fixed with ethanol:acetic acid (6:1) for 4 h and were washed with 100% ethanol three times and then 70% ethanol once. Finally, all tissues were cleared in a chloral hydrate solution (8 g of chloral hydrate, 1 mL of glycerol, and 2 mL of distilled water) and mounted on slide glass. The microscopic images were obtained using a differential interference contrast microscope (Zeiss Axioplan). Subepidermal cells aligned along a longitudinal axis just beside the midvein or along a transverse axis in the maximum width region were counted. To determine cell area, 20 cells grouped halfway from the midvein to the leaf margin at the widest point were analyzed with SCIONIMAGE software.
Mature embryos were prepared and stained with propidium iodide according to Running et al. (1995) Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers AY102639 through AY102641 for GIF1 through GIF3, respectively.
The following materials are available in the online version of this article.
We thank Dr. Woo Taek Kim for technical support, critical reading of the manuscript, and helpful comments; Dr. Myeong Min Lee for technical support; and Drs. Soon Ki Park and Jong Tae Song for sharing their growth room. We also thank the Arabidopsis Biological Resource Center for the mutant seeds. Received May 21, 2009; accepted July 27, 2009; published July 31, 2009.
1 This work was supported by the Korea Research Foundation (grant nos. KRF–2006–331–C00264 and KRF–2008–314–C00345).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jeong Hoe Kim (kimjeon4{at}knu.ac.kr).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.141838 * Corresponding author; e-mail kimjeon4{at}knu.ac.kr.
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catalyses translesion synthesis and interacts functionally with PCNA2. Plant J 55: 895–908
