Promotion of chloroplast proliferation upon enhanced post-mitotic cell expansion in leaves
© Kawade et al.; licensee BioMed Central Ltd. 2013
Received: 2 September 2013
Accepted: 20 September 2013
Published: 28 September 2013
Leaves are determinate organs; hence, precise control of cell proliferation and post-mitotic cell expansion is essential for their growth. A defect in cell proliferation often triggers enhanced post-mitotic cell expansion in leaves. This phenomenon is referred to as ‘compensation’. Several lines of evidence from studies on compensation have shown that cell proliferation and post-mitotic cell expansion are coordinately regulated during leaf development. Therefore, compensation has attracted much attention to the mechanisms for leaf growth. However, our understanding of compensation at the subcellular level remains limited because studies of compensation have focused mainly on cellular-level phenotypes. Proper leaf growth requires quantitative control of subcellular components in association with cellular-level changes. To gain insight into the subcellular aspect of compensation, we investigated the well-known relationship between cell area and chloroplast number per cell in compensation-exhibiting lines, and asked whether chloroplast proliferation is modulated in response to the induction of compensation.
We first established a convenient and reliable method for observation of chloroplasts in situ. Using this method, we analyzed Arabidopsis thaliana mutants fugu5 and angustifolia3 (an3), and a transgenic line KIP-RELATED PROTEIN2 overexpressor (KRP2 OE), which are known to exhibit typical features of compensation. We here showed that chloroplast number per cell increased in the subepidermal palisade tissue of these lines. We analyzed tetraploidized wild type, fugu5, an3 and KRP2 OE, and found that cell area itself, but not nuclear ploidy, is a key parameter that determines the activity of chloroplast proliferation. In particular, in the case of an3, we uncovered that promotion of chloroplast proliferation depends on the enhanced post-mitotic cell expansion. The expression levels of chloroplast proliferation-related genes are similar to or lower than that in the wild type during this process.
This study demonstrates that chloroplast proliferation is promoted in compensation-exhibiting lines. This promotion of chloroplast proliferation takes place in response to cell-area increase in post-mitotic phase in an3. The expression of chloroplast proliferation-related genes were not promoted in compensation-exhibiting lines including an3, arguing that an as-yet-unknown mechanism is responsible for modulation of chloroplast proliferation in these lines.
KeywordsCell area Chloroplast number per cell Compensation Leaf growth Nuclear ploidy
Leaf growth is driven by spatiotemporal control of cell proliferation and post-mitotic cell expansion. In the early developmental stage, cell proliferation actively occurs throughout leaf primordia. The proliferating region is maintained within a constant distance from the leaf base, then abruptly disappeared from distal to proximal regions of the leaf blade [1–5]. After arrest of mitotic cycling, cells show post-mitotic expansion with an intense increase in vacuolar volume. During leaf development, a defect in cell proliferation often triggers enhanced post-mitotic cell expansion. This phenomenon is termed ‘compensation’ [6–8] and is widely observed in seed plants including Arabidopsis thaliana (hereafter Arabidopsis) and Oryza sativa [9–11]. Interestingly, our recent study of compensation revealed that the two driving forces of leaf growth —proliferation and post-mitotic expansion of cells— are coordinately regulated during development . Compensation is therefore considered to be a key phenomenon for understanding the control of leaf growth.
Enhanced post-mitotic cell expansion could be detected by observing leaf cells from a paradermal view and measuring their area. Kinetics of the cell-area changes indicated that increase in cell area takes place in three distinct manner in compensation-exhibiting lines represented by angustifolia3 (an3) (enhanced rate of post-mitotic cell expansion), fugu5 (prolonged post-mitotic cell expansion) and a cyclin dependent kinase inhibitor gene KIP-RELATED PROTEIN2 overexpressor (KRP2 OE) (increase in cell area in both mitotic and post-mitotic phases) [10, 13]. The an3 is well characterized among compensation-exhibiting lines. The AN3 gene, also known as GRF-INTERACTING FACTOR1, encodes a transcriptional co-activator for leaf cell proliferation in Arabidopsis [14–16]. In the an3 leaves, cell number is decreased by more than 70% but cell area is increased by 50% when compared with the WT [10, 15–17]. For induction of enhanced post-mitotic cell expansion, a decrease in cell proliferation below a threshold is required . This fact suggests that enhanced post-mitotic cell expansion in an3 is not a simple result of a defect in cell proliferation, but a result of an active motion for leaf growth in response to a defect in cell proliferation. This idea is supported by our recent analysis of chimeric leaves for AN3 expression: an3 mutant cells are considered to actively produce and transmit an inter-cellular signal for enhanced post-mitotic cell expansion . These studies have deepened our understanding of the mechanism of compensation, and hence leaf growth, at the cellular level.
On the other hand, subcellular aspects in compensation-exhibiting lines including an3 have received less attention. Quantitative control of subcellular components is required for the proper functioning of leaf cells. Anatomical studies have revealed that the number of chloroplasts per cell is correlated with cell area [19–21]. In this study, we investigated the number of chloroplasts per cell in compensation-exhibiting lines to address whether subcellular aspect is affected in response to the induction of compensation.
Chloroplasts are derived from proplastids in meristematic cells, and multiply by division during leaf development. Two paralogous nucleus-encoded genes PLASTID DIVISION1 (PDV1) and PDV2 are involved in the chloroplast proliferation [22–24]. The expression for PDV1 and PDV2 in Arabidopsis occurs in the shoot apical meristem and in young leaf primordia, and then decreases in parallel with cessation of chloroplast proliferation [23, 24]. Importantly, overexpression of PDV1 and/or PDV2 increases the number of chloroplasts, while a loss-of-function mutation in PDV1 and/or PDV2 has the opposite effect [22–24]. Other components involved in chloroplast proliferation have been also identified such as self-assembling cytoskeletal GTPase genes Filamentous temperature sensitive Z1 (FtsZ1) and FtsZ2 , a gene encoding J-domain containing protein ACCUMULATION AND REPLICATION OF CHLOROPLASTS 6 (ARC6) , Min system-related genes [MinC, MinD, MinE and MULTIPLE CHLOROPLAST DIVISION SITE 1 (MCD1)] [27, 28]. Although involvement of these genes into chloroplast proliferation is apparent, it is known that overexpression or knockdown/knockout of them does not promote chloroplast proliferation [25–31]. Therefore, the extent of chloroplast proliferation depends primarily on the expression levels of PDVs. It is worth investigating the expression level of PDVs in compensation-exhibiting lines to determine whether chloroplast proliferation is modulated in response to the induction of compensation.
We here established a convenient method for counting chloroplasts in subepidermal palisade cells in situ. By use of this method, we investigate the relationship between cell area and chloroplast number per cell in compensation-exhibiting lines. Based on our results, we discuss the promotion of chloroplast proliferation in response to the enhanced post-mitotic cell expansion. In addition, we discuss whether the promotion of chloroplast proliferation occurs through an up-regulation of the expression levels of PDVs.
Results and discussion
Establishment of a method for counting chloroplasts in situ
Chloroplast number per cell increased in the leaves of compensation-exhibiting lines
Chloroplast proliferation activity decreases with developmental progression in WT leaves . On the other hand, our data indicate that the number of chloroplasts per cell is correlated with final cell area in the mature leaves, which is determined through the post-mitotic cell expansion. Mitotic cell area in 5-day-old fugu5-1 and an3-4 lines is similar to that in the WT (Figure 2C) , supporting our idea that chloroplast proliferation is modulated in response to the status of post-mitotic cell expansion in these mutants. We should carefully consider the contribution of post-mitotic cell expansion to promotion of chloroplast proliferation in KRP2 OE, because area of mitotic cells in this line is about two fold larger than that in WT (Figure 2C) [10, 13]. Therefore, chloroplast proliferation could be modulated also during mitotic phase of leaf cells. Establishment of method for precise enumeration of immature chloroplasts in mitotic cells would be helpful to further investigate this issue.
Relationship between final cell area, nuclear ploidy and chloroplast number per cell
Nuclear ploidy is increased through not only endoreduplication but also polyploidization. To further investigate the effect of increased nuclear ploidy on chloroplast proliferation, we established tetraploidized WT, fugu5-1, an3-4 and KRP2 OE lines (Figure 3B) and analyzed their leaves 21 days after sowing. We found that chloroplast number per cell increased by 55%, 43%, 53% and 15% in tetraploid WT, fugu5-1, an3-4 and KRP2 OE, respectively, when compared with diploid counterparts (Figure 3C). These rates of increase are different from that expected (100%) if chloroplast number per cell was linearly correlated with nuclear ploidy. Rather, these rates of increase are similar to those of cell area: in tetraploid WT, fugu5-1, an3-4 and KRP2 OE, cell areas increased by 69%, 34% 42% and 14%, respectively, compared to their diploid counterparts (Figure 3C). Together, we conclude that nuclear ploidy does not directly affect chloroplast proliferation, and final cell area is the key parameter for chloroplast proliferation.
Enhanced post-mitotic cell expansion is required for promotion of chloroplast proliferation in an3
Chloroplast proliferation is promoted in compensation-exhibiting lines without up-regulation of the expression of PDVs
It was previously believed that expression level of PDVs determines the rate of chloroplast proliferation because increased or decreased level of PDVs expression lead to an increase or decrease in chloroplast proliferation, respectively [23, 24]. The expression for PDVs decreases along with leaf development in the WT, whereas our data indicate that chloroplast proliferation is promoted in response to increase in cell area. This fact suggests that the control of chloroplast proliferation might be more flexible than previously thought in response to the change in final cell area. If that is the case, whether the expression level of PDVs is up-regulated in response to cell-area change in leaves of compensation-exhibiting lines is an important question.
In this study we reported a reliable method for chloroplast enumeration in situ and demonstrated that chloroplast number per cell increases in compensation-exhibiting lines. Nuclear ploidy is not directly involved in the control of chloroplast proliferation in compensation-exhibiting lines. Of particular note is the finding that chloroplast proliferation is modulated during leaf development in response to the status of post-mitotic cells. In this process, the expression of PDVs and other chloroplast proliferation-related genes were not up-regulated, arguing an as-yet-unknown mechanism for promotion of chloroplast proliferation in response to cell-area change. These findings highlight a novel aspect of compensation, and, therefore, provide important insight into the fundamental understanding of leaf growth.
Plant materials and growth conditions
The WT accession of Arabidopsis used in this study was Columbia-0. Tetraploidization of WT, fugu5-1, an3-4 and KRP2 OE lines were carried out as described previously , followed by flowcytometory analysis to confirm their nuclear ploidy . Plants were grown on rock wool at 22°C under 16 h light/8 h dark, and watered daily with 0.5 g L-1 Hyponex solution. Light at approximately 50 μmol m-2 s-1 was provided by white fluorescent lamps.
The first leaves from 21-day-old plants are infiltrated with 0.05% (v/v) Triton X-100 and 1% (v/v) glycerol, and then counted the number of chloroplasts (n = 160 cells from 8 leaves for each line). Detailed method is described in the Results and Discussion section.
Measurement of cell area in leaves
After enumeration of chloroplast number per cell, the same leaf samples are subjected to analyze the cell area (n = 160 cells from 8 leaves for each line). Subepidermal palisade cells were observed under a light microscope (DMRX/E; Leica Microsystems). The leaf primordia was fixed in a formalin-acetic acid-alcohol (FAA) and cleared in a chloral hydrate solution (chloral hydrate, 200 g; glycerol 20 g; H2O, 50 ml) to measure the area of mitotic cells in the first leaves dissected from 5-day-old plants.
Quantification of transcripts of chloroplast proliferation-related genes by qRT-PCR
Total RNA was extracted from above-ground parts of 7-day-old seedlings and primordia of the first leaves in 14-day-old plants using RNeasy Plant mini kit (QIAGEN) according to the manufacturer’s instructions. First-strand cDNA was synthesized from the extracted RNA using ReverTra Ace qPCR RT Master Mix with gDNA remover kit (TOYOBO). The PCR products were monitored by use of StepOnePlus real-time PCR system (Applied Biosystems) using Thunderbird SYBR qPCR mix (TOYOBO). Primers used were as follows: 5′ - CTTAACGCAATTCGAACCGC - 3′ and 5′ - TCCTGCTCTGTTCAAGCCG - 3′ for PDV1, 5′ - GCTGAACGGCTTTTGCGTAT - 3′ and 5′ - AATCAATCTCAGAGAGAGCCAGTTG - 3′ for PDV2, and 5′ - TCGGTGGTTCCATTCTTGCT - 3′ and 5′ - GCTTTTTAAGCCTTTGATCTTGAGAG - 3′ for ACTIN2, or as described elsewhere . The expression levels of chloroplast proliferation-related genes were normalized by that of ACTIN2 gene as an internal standard and expressed relative to the WT level (WT = 1). The specificity of PCR amplification was examined by monitoring the melting curves. Data were obtained from three independent biological replicates with triplicates in each sample, and were analyzed statistically.
We thank U. Fujikura (Potsdom Univ.) for his advice on the observation of chloroplasts. This work was supported by grants-in-aid for Creative Scientific Research (No. 18GS0313 to H.T.), Scientific Research on Priority Areas (No. 19060002 to H.T.), Scientific Research A (No. 17207005 to H.T. and G.H.), Exploratory Research (No. 18657020 to G.H.), Scientific Research on Innovative Areas (No. 25113002 to H.T. and No. 25113010 to M.Y.H.), a fellowship from the Japan Society for the Promotion of Science (JSPS) (No. 217214 to K.K.), the RIKEN Special Postdoctoral Researchers Program (No. K23253 to K.K.) and the Toray Science Foundation (to H.T.).
- Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG: Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol. 1999, 215 (2): 407-419. 10.1006/dbio.1999.9443.PubMedView ArticleGoogle Scholar
- Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H: Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiol. 2011, 157 (3): 1151-1162. 10.1104/pp.111.185066.PubMedPubMed CentralView ArticleGoogle Scholar
- Kazama T, Ichihashi Y, Murata S, Tsukaya H: The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. Plant Cell Physiol. 2010, 51 (6): 1046-1054. 10.1093/pcp/pcq051.PubMedView ArticleGoogle Scholar
- Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Muhlenbock P, Skirycz A, Gonzalez N, Beemster GT, et al: Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell. 2012, 22 (1): 64-78. 10.1016/j.devcel.2011.11.011.PubMedView ArticleGoogle Scholar
- White DW: PEAPOD regulates lamina size and curvature in Arabidopsis. Proc Natl Acad Sci U S A. 2006, 103 (35): 13238-13243. 10.1073/pnas.0604349103.PubMedPubMed CentralView ArticleGoogle Scholar
- Beemster GT, Fiorani F, Inze D: Cell cycle: the key to plant growth control?. Trends Plant Sci. 2003, 8 (4): 154-158. 10.1016/S1360-1385(03)00046-3.PubMedView ArticleGoogle Scholar
- Tsukaya H: Interpretation of mutants in leaf morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theories. Int Rev Cytol. 2002, 217: 1-39.PubMedView ArticleGoogle Scholar
- Tsukaya H: Controlling size in multicellular organs: focus on the leaf. PLoS Biol. 2008, 6: 1373-1376.View ArticleGoogle Scholar
- Barrôco RM, Peres A, Droual AM, De Veylder L, le Nguyen SL, De Wolf J, Mironov V, Peerbolte R, Beemster GT, Inze D, Broekaert WF, Frankard V: The cyclin-dependent kinase inhibitor Orysa; KRP1 plays an important role in seed development of rice. Plant Physiol. 2006, 142 (3): 1053-1064. 10.1104/pp.106.087056.PubMedPubMed CentralView ArticleGoogle Scholar
- Ferjani A, Horiguchi G, Yano S, Tsukaya H: Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol. 2007, 144 (2): 988-999. 10.1104/pp.107.099325.PubMedPubMed CentralView ArticleGoogle Scholar
- Horiguchi G, Tsukaya H: Organ size regulation in plants: insights from compensation. Front Plant Sci. 2011, 2: 24-PubMedPubMed CentralView ArticleGoogle Scholar
- Kawade K, Horiguchi G, Tsukaya H: Non-cell-autonomously coordinated organ size regulation in leaf development. Development. 2010, 137 (24): 4221-4227. 10.1242/dev.057117.PubMedView ArticleGoogle Scholar
- De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inze D: Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell. 2001, 13 (7): 1653-1668.PubMedPubMed CentralView ArticleGoogle Scholar
- Kim JH, Kende H: A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci U S A. 2004, 101 (36): 13374-13379. 10.1073/pnas.0405450101.PubMedPubMed CentralView ArticleGoogle Scholar
- Horiguchi G, Kim GT, Tsukaya H: The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J. 2005, 43 (1): 68-78. 10.1111/j.1365-313X.2005.02429.x.PubMedView ArticleGoogle Scholar
- Kawade K, Horiguchi G, Usami T, Hirai MY, Tsukaya H: ANGUSTIFOLIA3 signaling coordinates proliferation between clonally distinct cells in leaves. Curr Biol. 2013, 23 (9): 788-792. 10.1016/j.cub.2013.03.044.PubMedView ArticleGoogle Scholar
- Fujikura U, Horiguchi G, Tsukaya H: Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol. 2007, 48 (2): 278-286.PubMedView ArticleGoogle Scholar
- Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H: Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana. Plant J. 2009, 59 (3): 499-508. 10.1111/j.1365-313X.2009.03886.x.PubMedView ArticleGoogle Scholar
- Pyke KA, Leech RM: Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) Heynh. Plant Physiol. 1991, 96 (4): 1193-1195. 10.1104/pp.96.4.1193.PubMedPubMed CentralView ArticleGoogle Scholar
- Pyke KA, Leech RM: Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol. 1992, 99 (3): 1005-1008. 10.1104/pp.99.3.1005.PubMedPubMed CentralView ArticleGoogle Scholar
- Pyke KA, Leech RM: A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol. 1994, 104 (1): 201-207.PubMedPubMed CentralGoogle Scholar
- Miyagishima SY, Froehlich JE, Osteryoung KW: PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell. 2006, 18 (10): 2517-2530. 10.1105/tpc.106.045484.PubMedPubMed CentralView ArticleGoogle Scholar
- Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, Matsui M, Nakanishi H, Miyagishima SY: The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell. 2009, 21 (6): 1769-1780. 10.1105/tpc.109.067785.PubMedPubMed CentralView ArticleGoogle Scholar
- Okazaki K, Kabeya Y, Miyagishima SY: The evolution of the regulatory mechanism of chloroplast division. Plant Signal Behav. 2010, 5 (2): 164-167. 10.4161/psb.5.2.10461.PubMedPubMed CentralView ArticleGoogle Scholar
- Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY: Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell. 1998, 10 (12): 1991-2004.PubMedPubMed CentralGoogle Scholar
- Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW: ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell. 2003, 15 (8): 1918-1933. 10.1105/tpc.013292.PubMedPubMed CentralView ArticleGoogle Scholar
- Nakanishi H, Suzuki K, Kabeya Y, Miyagishima SY: Plant-specific protein MCD1 determines the site of chloroplast division in concert with bacteria-derived MinD. Curr Biol. 2009, 19 (2): 151-156. 10.1016/j.cub.2008.12.018.PubMedView ArticleGoogle Scholar
- Yang Y, Glynn JM, Olson BJSC, Schmitz AJ, Osteryoung KW: Plastid division: across time and space. Curr Opin Plant Biol. 2008, 11: 577-584. 10.1016/j.pbi.2008.10.001.PubMedView ArticleGoogle Scholar
- Stokes KD, McAndrew RS, Figueroa R, Vitha S, Osteryoung KW: Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis. Plant Physiol. 2000, 124 (4): 1668-1677. 10.1104/pp.124.4.1668.PubMedPubMed CentralView ArticleGoogle Scholar
- Collettie KS, Tattersall EA, Pyke KA, Froelich JE, Stoke KD, Osteryound KW: A homologue of the bacterial cell division site-determining factor MinD mediates plavement of the chloroplast division apparatus. Curr Biol. 2000, 10 (9): 507-516. 10.1016/S0960-9822(00)00466-8.View ArticleGoogle Scholar
- Itoh R, Fujiwara M, Nagata N, Yoshida S: A chloroplast protein homologus to the eubacterial topological specificity factor MinE plays a role in chloroplast division. Plant Physiol. 2001, 127 (4): 1644-1655. 10.1104/pp.010386.PubMedPubMed CentralView ArticleGoogle Scholar
- Melaragno JE, Mehrotra B, Coleman AW: Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell. 1993, 5 (11): 1661-1668.PubMedPubMed CentralView ArticleGoogle Scholar
- Castellano MM, Boniotti MB, Caro E, Schnittger A, Gutierrez C: DNA replication licensing affects cell proliferation or endoreplication in a cell type-specific manner. Plant Cell. 2004, 16 (9): 2380-2393. 10.1105/tpc.104.022400.View ArticleGoogle Scholar
- Raynaud C, Perennes C, Reuzeau C, Catrice O, Brown S, Bergounioux C: Cell and plastid division are coordinated through the prereplication factor AtCDT1. Proc Natl Acad Sci U S A. 2005, 102 (23): 8216-8221. 10.1073/pnas.0502564102.PubMedPubMed CentralView ArticleGoogle Scholar
- Verkest A, Manes CLO, Vercruysse S, Maes S, Schueren EVD, Beeckman T, Genschik P, Kuiper M, Inze D, De Veylder L: The Cyclin-dependent kinease inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA; 1 kinase complexes. Plant Cell. 2005, 17 (6): 1723-1736. 10.1105/tpc.105.032383.PubMedPubMed CentralView ArticleGoogle Scholar
- Breuer C, Stacey NJ, West CE, Zhao Y, Chory J, Tsukaya H, Azumi Y, Maxwell A, Roberts K, Sugimoto-Shirasu K: BIN4, a novel component of the plant DNA topoisomerase VI complex, is required for endoreduplication in Arabidopsis. Plant Cell. 2007, 19 (11): 3655-3668. 10.1105/tpc.107.054833.PubMedPubMed CentralView ArticleGoogle Scholar
- Kozuka T, Horiguchi G, Kim GT, Ohgishi M, Sakai T, Tsukaya H: The different growth responses of the Arabidopsis thaliana leaf blade and the petiole during shade avoidance are regulated by photoreceptors and sugar. Plant Cell Physiol. 2005, 46 (1): 213-223. 10.1093/pcp/pci016.PubMedView ArticleGoogle Scholar
- Nobusawa T, Umeda M: Very-long-chain fatty acids have an essential role in plastid division by controlling Z-ring formation in Arabidopsis thaliana. Genes Cells. 2012, 17 (8): 709-719. 10.1111/j.1365-2443.2012.01619.x.PubMedView ArticleGoogle Scholar