Abstract
Plant organs grow to highly reproducible sizes that are determined by the plant's genotype and by the identity of the organ. The strong heritability of size differences indicates that organ size is under tight genetic control. The overall increase in size of plant organs is driven by two distinct processes: cell proliferation with the concomitant generation of cytoplasmic mass, and cell expansion due to water uptake into the central vacuole. Molecular genetic analysis has identified a number of genes that influence final organ size by acting on either of these two processes in a promoting or repressing manner. The differences in the sizes and shapes of the various organ types within individuals as well as the size differences among species result from the modification of growth patterns by factors controlling organ identity and by evolutionary change. Genetic analysis in model species is beginning to shed light on how these growth patterns are being controlled and modified. Together, these studies are unraveling how plant organs decide for or against further growth and suggest approaches for manipulating biomass accumulation in plants.
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References
Autran D, Jonak C, Belcram K, Beemster GT, Kronenberger J, Grandjean O, Inze D, Traas J (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21:6036–6049
Baldet P, Hernould M, Laporte F, Mounet F, Just D, Mouras A, Chevalier C, Rothan C (2006) The expression of cell proliferation-related genes in early developing flowers is affected by a fruit load reduction in tomato plants. J Exp Bot 57:961–970
Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141
Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967–971
Canales C, Grigg S, Tsiantis M (2005) The formation and patterning of leaves: recent advances. Planta 221:752–756
Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788
Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann KA (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J 26:573–582
Choi D, Lee Y, Cho HT, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398
Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451
Cnops G, Jover-Gil S, Peters JL, Neyt P, De Block S, Robles P, Ponce MR, Gerats T, Micol JL, Van Lijsebettens M (2004) The rotunda2 mutants identify a role for the LEUNIG gene in vegetative leaf morphogenesis. J Exp Bot 55:1529–1539
Cockcroft CE, den Boer BG, Healy JM, Murray JA (2000) Cyclin D control of growth rate in plants. Nature 405:575–579
Cong B, Liu J, Tanksley SD (2002) Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. Proc Natl Acad Sci USA 99:13606–13611
Corley SB, Carpenter R, Copsey L, Coen E (2005) Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Natl Acad Sci USA 102:5068–5073
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
Costa MM, Fox S, Hanna AI, Baxter C, Coen E (2005) Evolution of regulatory interactions controlling floral asymmetry. Development 132:5093–5101
Crawford BC, Nath U, Carpenter R, Coen ES (2004) CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of Antirrhinum. Plant Physiol 135:244–253
De Veylder L, Beeckman T, Beemster GT, de Almeida Engler J, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G et al. (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 21:1360–1368
De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inze D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668
del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18:2224–2235
Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92
Dinneny JR, Weigel D, Yanofsky MF (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development 132:4687–4696
Dinneny JR, Weigel D, Yanofsky MF (2006) NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 133:1645–1655
Dinneny JR, Yadegari R, Fischer RL, Yanofsky MF, Weigel D (2004) The role of JAGGED in shaping lateral organs. Development 131:1101–1110
Disch S, Anastasiou E, Sharma VK, Laux T, Fletcher JC, Lenhard M (2006) The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr Biol 16:272–279
Doerner P, Jorgensen JE, You R, Steppuhn J, Lamb C (1996) Control of root growth and development by cyclin expression. Nature 380:520–523
Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419
Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168
Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574
Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85
Franks RG, Liu Z, Fischer RL (2006) SEUSS and LEUNIG regulate cell proliferation, vascular development and organ polarity in Arabidopsis petals. Planta 224(4):801–811
Franks RG, Wang C, Levin JZ, Liu Z (2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129:253–263
Frary A, Fritz LA, Tanksley SD (2004) A comparative study of the genetic bases of natural variation in tomato leaf, sepal, and petal morphology. Theor Appl Genet 109:523–533
Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
Gaudin V, Lunness PA, Fobert PR, Towers M, Riou-Khamlichi C, Murray JA, Coen E, Doonan JH (2000) The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol 122:1137–1148
Ha CM, Jun JH, Nam HG, Fletcher JC (2004) BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 45:1361–1370
Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG (2003) The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130:161–172
Hepworth SR, Zhang Y, McKim S, Li X, Haughn GW (2005) BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. Plant Cell 17:1434–1448
Horiguchi G, Ferjani A, Fujikura U, Tsukaya H (2006) Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. J Plant Res 119:37–42
Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78
Horvath BM, Magyar Z, Zhang Y, Hamburger AW, Bako L, Visser RG, Bachem CW, Bogre L (2006) EBP1 regulates organ size through cell growth and proliferation in plants. EMBO J 25:4909–4920
Hu Y, Poh HM, Chua NH (2006) The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth. Plant J 47:1–9
Hu Y, Xie Q, Chua NH (2003) The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15:1951–1961
Ingram GC, Waites R (2006) Keeping it together: co-ordinating plant growth. Curr Opin Plant Biol 9:12–20
Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C et al. (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478
Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5:887–896
Jünger T, Perez-Perez JM, Bernal S, Micol JL (2005) Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture. Evol Dev 7:259–271
Jünger T, Purugganan MD, Mackay TF (2000) Quantitative trait loci for floral morphology in Arabidopsis thaliana. Genetics 156:1379–1392
Kessler S, Sinha N (2004) Shaping up: the genetic control of leaf shape. Curr Opin Plant Biol 7:65–72
Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36:94–104
Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci USA 101:13374–13379
Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153
Krizek BA (1999) Ectopic expression of AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs. Dev Genet 25:224–236
Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698
Krizek BA, Sulli C (2006) Mapping sequences required for nuclear localization and the transcriptional activation function of the Arabidopsis protein AINTEGUMENTA. Planta 224:612–621
Langlade NB, Feng X, Dransfield T, Copsey L, Hanna AI, Thebaud C, Bangham A, Hudson A, Coen E (2005) Evolution through genetically controlled allometry space. Proc Natl Acad Sci USA 102:10221–10226
Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102:12978–12983
Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7:193–204
Liu J, Cong B, Tanksley SD (2003) Generation and analysis of an artificial gene dosage series in tomato to study the mechanisms by which the cloned quantitative trait locus fw2.2 controls fruit size. Plant Physiol 132:292–299
Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen E (1999) Control of organ asymmetry in flowers of Antirrhinum. Cell 99:367–376
Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799
Menand B, Robaglia C (2004) Plant cell growth. In: Hall MN (ed) Cell growth: control of cell size. Cold Spring Harbor Laboratory Press, New York, pp 625–637
Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539
Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947
Nath U, Crawford BC, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407
Nelissen H, Clarke JH, De Block M, De Block S, Vanderhaeghen R, Zielinski RE, Dyer T, Lust S, Inze D, Van Lijsebettens M (2003) DRL1, a homolog of the yeast TOT4/KTI12 protein, has a function in meristem activity and organ growth in plants. Plant Cell 15:639–654
Nole-Wilson S, Krizek BA (2006) AINTEGUMENTA contributes to organ polarity and regulates growth of lateral organs in combination with YABBY genes. Plant Physiol 141:977–987
Norberg M, Holmlund M, Nilsson O (2005) The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 132:2203–2213
Ohno CK, Reddy GV, Heisler MG, Meyerowitz EM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131:1111–1122
Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46
Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263
Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JW, Shaw PJ (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16:260–269
Perez-Perez JM, Serrano-Cartagena J, Micol JL (2002) Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. Genetics 162:893–915
Richards DE, King KE, Ait-Ali T, Harberd NP (2001) HOW GIBBERELLIN REGULATES PLANT GROWTH AND DEVELOPMENT: a molecular genetic analysis of gibberellin signaling. Annu Rev Plant Physiol Plant Mol Biol 52:67–88
Riefler M, Novak O, Strnad M, Schmulling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54
Rudra D, Warner JR (2004) What better measure than ribosome synthesis? Genes Dev 18:2431–2436
Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103
Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261
Schwarz-Sommer Z, Davies B, Hudson A (2003) An everlasting pioneer: the story of Antirrhinum research. Nat Rev Genet 4:657–666
Scofield S, Murray JA (2006) KNOX gene function in plant stem cell niches. Plant Mol Biol 60:929–946
Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131:1491–1501
Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293
Shuai B, Reynaga-Pena CG, Springer PS (2002) The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761
Sonnewald U, Hajirezaei MR, Kossmann J, Heyer A, Trethewey RN, Willmitzer L (1997) Increased potato tuber size resulting from apoplastic expression of a yeast invertase. Nat Biotechnol 15:794–797
Sridhar VV, Surendrarao A, Gonzalez D, Conlan RS, Liu Z (2004) Transcriptional repression of target genes by LEUNIG and SEUSS, two interacting regulatory proteins for Arabidopsis flower development. Proc Natl Acad Sci USA 101:11494–11499
Sugimoto-Shirasu K, Roberts GR, Stacey NJ, McCann MC, Maxwell A, Roberts K (2005) RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc Natl Acad Sci USA 102:18736–18741
Sugimoto-Shirasu K, Roberts K (2003) Big it up: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6:544–553
Sugimoto-Shirasu K, Stacey NJ, Corsar J, Roberts K, McCann MC (2002) DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr Biol 12:1782–1786
Szecsi J, Joly C, Bordji K, Varaud E, Cock JM, Dumas C, Bendahmane M (2006) BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size. EMBO J 25:3912–3920
Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altmann T, Redei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171–182
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543
Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13:3378–3388
Veit B (2006) Stem cell signalling networks in plants. Plant Mol Biol 60:793–810
Vert G, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177–201
Waites R, Hudson A (1995) Phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154
Waites R, Selvadurai HR, Oliver IR, Hudson A (1998) The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93:779–789
Weijers D, Franke-van Dijk M, Vencken RJ, Quint A, Hooykaas P, Offringa R (2001) An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128:4289–4299
Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550
Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492
White DW (2006) PEAPOD regulates lamina size and curvature in Arabidopsis. Proc Natl Acad Sci USA 103:13238–13243
Zenoni S, Reale L, Tornielli GB, Lanfaloni L, Porceddu A, Ferrarini A, Moretti C, Zamboni A, Speghini A, Ferranti F et al. (2004) Downregulation of the Petunia hybrida alpha-expansin gene PhEXP1 reduces the amount of crystalline cellulose in cell walls and leads to phenotypic changes in petal limbs. Plant Cell 16:295–308
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Anastasiou, E., Lenhard, M. (2008). Control of Plant Organ Size. In: Bögre, L., Beemster, G. (eds) Plant Growth Signaling. Plant Cell Monographs, vol 10. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2007_149
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