Molecular Mechanisms Affecting Cell Wall Properties and Leaf Architecture

  • Sarathi M. Weraduwage
  • Marcelo L. Campos
  • Yuki Yoshida
  • Ian T. Major
  • Yong-Sig Kim
  • Sang-Jin Kim
  • Luciana Renna
  • Fransisca C. Anozie
  • Federica Brandizzi
  • Michael F. Thomashow
  • Gregg A. Howe
  • Thomas D. SharkeyEmail author
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)


Leaf architecture is determined by cell shape, size, and density. As plant cells are enclosed by a rigid cell wall, changes to leaf architecture have to occur through downstream genetic systems that induce alterations in (1) cell wall composition, (2) synthesis, assembly, and orientation of cytoskeletal elements and/or (3) the degree of cross-linkage between wall components in response to upstream developmental and environmental cues. This chapter reviews how leaf architecture is influenced by molecular mechanisms that modulate the above wall modification processes. Upstream signaling systems such as salicylic (SA), jasmonic (JA), and gibberellic (GA) acid have significant effects on leaf architecture. GA promotes and JA and SA suppress growth. Leaf architectural changes are brought about by these upstream systems in concert or in an interactive manner, and the associated downstream molecular systems that are involved in executing changes to cell wall properties will be discussed. Evidence will be provided to show that xyloglucan endotransglucosylase/hydrolase and pectin methyltransferase/pectin methylesterase/pectin methylesterase inhibitor systems are key downstream execution points of leaf architectural changes common to different upstream molecular systems. Optimization of leaf architecture maximizes light interception, gas exchange properties, and photosynthesis. In addition, plant growth has been shown to be more sensitive to leaf area than to area-based photosynthesis rate. Therefore, understanding genes and molecular mechanisms that affect cell wall properties and leaf architecture has broader implications in terms of crop improvement, and candidate genes that can be manipulated to optimize leaf architecture in order to maximize net carbon assimilation and plant growth will be proposed.



abscisic acid




alcohol insoluble residue






















cgr2/3 complemented by CGR2


CGR2 overexpression line of Arabidopsis thaliana


carbon dioxide










PIF transcription factor repressors


dehydration responsive element




actin microfilaments




gibberellic acid








basic helix-loop-helix subgroup IIIe transcription factors


jasmonic acid


jasmonate ZIM-domain repressors


JAZ quintuple mutation


leaf dry mass per unit leaf area


leaf mass density








fine actin filament






a basic helix-loop-helix transcription factor






polymerase chain reaction


active form of phytochrome that absorbs far-red light




phytochrome-interacting factors








pectin methyltransferase


inactive form of phytochrome that absorbs red light


potato virus X vector






negative regulator of ROP


Rho-guanine nucleotide exchange factors




RNA sequencing






ribulose bisphosphate carboxylase oxygenase


salicylic acid






chloroplast surface area facing intercellular air spaces per unit leaf area




salicylic acid induction-deficient 2-1


small interfering RNA


mesophyll cell surface area facing intercellular air spaces per unit leaf area










virus-induced gene silencing


Vienna-Pee-Dee Belemnite standard












ratio of 13C to 12C isotopes in leaf tissue relative to a Vienna-Pee-Dee Belemnite standard



We are grateful to Drs. Sean E. Weise, (Department of Biochemistry and Molecular Biology), Cliff Foster (the Cell Wall Facility, Great Lakes Bioenergy Research Center), Alicia Withrow and Melinda Frame (Center for Advanced Microscopy) of Michigan State University (East Lansing, MI), and to Dr. Suvankar Chakraborty (Stable Isotope Ratio Facility for Environmental Research) of the University of Utah (Salt Lake City, UT) for their support. We also wish to thank Jim Klug and Cody Keilen (Growth Chamber Facility) of Michigan State University for their assistance and all members of the Brandizzi, Thomashow, Howe, and Sharkey labs for their support. Funding for this research was provided by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U. S. Department of Energy (award number DE-FG02-91ER20021) and in part by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494). Partial salary support for MT, GH, TDS, and FB came from Michigan AgBioResearch.


  1. Achard P, Liao L, Jiang C, Desnos T, Bartlett J, Fu X, Harberd NP (2007) DELLAs contribute to plant photomorphogenesis. Plant Physiol 143:1163–1172PubMedPubMedCentralCrossRefGoogle Scholar
  2. An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W et al (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720PubMedCrossRefGoogle Scholar
  4. Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222PubMedCrossRefGoogle Scholar
  5. Basu D, Le J, El-Essal SE, Huang S, Zhang C, Mallery EL et al (2005) DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell 17:502–524PubMedPubMedCentralCrossRefGoogle Scholar
  6. Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB (2008) A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. Proc Natl Acad Sci U S A 105:4044–4049PubMedPubMedCentralCrossRefGoogle Scholar
  7. Becnel J, Natarajan M, Kipp A, Braam J (2006) Developmental expression patterns of Arabidopsis XTH genes reported by transgenes and Genevestigator. Plant Mol Biol 61:451–467PubMedCrossRefGoogle Scholar
  8. Beeckman T, Przemeck GKH, Stamatiou G, Lau R, Terryn N, De Rycke R et al (2002) Genetic complexity of cellulose synthase a gene function in Arabidopsis embryogenesis. Plant Physiol 130:1883–1893PubMedPubMedCentralCrossRefGoogle Scholar
  9. Behringer C, Schwechheimer C (2015) B-GATA transcription factors – insights into their structure, regulation and role in plant development. Front Plant Sci 6:90PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bouton S, Leboeuf E, Mouille G, Leydecker MT, Talbotec J, Granier F et al (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14:2577–2590PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141PubMedCrossRefGoogle Scholar
  12. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and Molecular Biology of Plants. Wiley, SomersetGoogle Scholar
  13. Burton RA, Gibeaut DM, Bacic A, Findlay K, Roberts K, Hamilton A et al (2000) Virus-induced silencing of a plant cellulose synthase gene. Plant Cell 12:691–705PubMedPubMedCentralCrossRefGoogle Scholar
  14. Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236PubMedPubMedCentralCrossRefGoogle Scholar
  15. Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A et al (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-β-d-glucans. Science 311:1940–1942PubMedCrossRefGoogle Scholar
  16. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900PubMedCrossRefGoogle Scholar
  17. Campos ML, Yoshida Y, Major IT, de Oliveira Ferreira D, Weraduwage SM et al (2016) Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat Commun 7:12570PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chaiwanon J, Wang W, Zhu J-Y, Oh E, Wang Z-Y (2016) Information integration and communication in plant growth regulation. Cell 164:1257–1268PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chan J (2012) Microtubule and cellulose microfibril orientation during plant cell and organ growth. J Microsc 247:23–32PubMedCrossRefGoogle Scholar
  20. Chan Z, Grumet R, Loescher W (2011) Global gene expression analysis of transgenic, mannitol-producing, and salt-tolerant Arabidopsis thaliana indicates widespread changes in abiotic and biotic stress-related genes. J Exp Bot 62:4787–4803PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chapman EJ, Greenham K, Castillejo C, Sartor R, Bialy A, Sun TP, Estelle M (2012) Hypocotyl transcriptome reveals auxin regulation of growth-promoting genes through GA-dependent and -independent pathways. PLoS One 7:9Google Scholar
  22. Chen M-H, Sheng J, Hind G, Handa AK, Citovsky V (2000) Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J 19:913–920PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cho SK, Kim JE, Park JA, Eom TJ, Kim WT (2006) Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett 580:3136–3144PubMedCrossRefGoogle Scholar
  24. Choe S, Tanaka A, Noguchi T, Fujioka S, Takatsuto S, Ross AS et al (2000) Lesions in the sterol Δ7 reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J 21:431–443PubMedCrossRefGoogle Scholar
  25. Chou Y-H, Pogorelko G, Zabotina OA (2012) Xyloglucan xylosyltransferases XXT1, XXT2, and XXT5 and the glucan synthase CSLC4 form Golgi-localized multiprotein complexes. Plant Physiol 159:1355–1366PubMedPubMedCentralCrossRefGoogle Scholar
  26. Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75PubMedCrossRefGoogle Scholar
  27. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedPubMedCentralCrossRefGoogle Scholar
  28. Craddock C, Lavagi I, Yang Z (2012) New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol 22:492–501PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecol Monogr 69:569–588CrossRefGoogle Scholar
  30. Cutler JM, Rains DW, Loomis RS (1977) The importance of cell size in the water relations of plants. Physiol Plant 40:255–260CrossRefGoogle Scholar
  31. de Vries RP, Visser J (2001) Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev 65:497–522PubMedPubMedCentralCrossRefGoogle Scholar
  32. Dijkstra P, Reegen H, Kuiper PJ (1990) Relation between relative growth rate, endogenous gibberellins, and the response to applied gibberellic acid for Plantago major. Physiol Plant 79:629–634PubMedCrossRefGoogle Scholar
  33. Djakovic S, Dyachok J, Burke M, Frank MJ, Smith LG (2006) BRICK1/HSPC300 functions with SCAR and the ARP2/3 complex to regulate epidermal cell shape in Arabidopsis. Development 133:1091–1100PubMedCrossRefGoogle Scholar
  34. Doblin MS, Pettolino FA, Wilson SM, Campbell R, Burton RA, Fincher GB et al (2009) A barley cellulose synthase-like CSLH gene mediates (1,3;1,4)-β-D-glucan synthesis in transgenic Arabidopsis. Proc Natl Acad Sci U S A 106:5996–6001PubMedPubMedCentralCrossRefGoogle Scholar
  35. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984PubMedPubMedCentralCrossRefGoogle Scholar
  36. Dwivany FM, Yulia D, Burton RA, Shirley NJ, Wilson SM, Fincher GB et al (2009) The CELLULOSE-SYNTHASE LIKE C (CSLC) family of barley includes members that are integral membrane proteins targeted to the plasma membrane. Mol Plant 2:1025–1039PubMedCrossRefGoogle Scholar
  37. Ellis B, Daly DC, Hickey LJ, Mitchell JV, Johnson KR, Wilf P, Wing SL (2009) Manual of Leaf Architecture. Cornell University Press, IthacaGoogle Scholar
  38. Eriksson EM, Bovy A, Manning K, Harrison L, Andrews J, De Silva J et al (2004) Effect of the colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol 136:4184–4197PubMedPubMedCentralCrossRefGoogle Scholar
  39. Ferjani A, Horiguchi G, Yano S, Tsukaya H (2007) Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol 144:988–999PubMedPubMedCentralCrossRefGoogle Scholar
  40. Filisetti-Cozzi TM, Carpita NC (1991) Measurement of uronic acids without interference from neutral sugars. Anal Biochem 197:157–162PubMedCrossRefGoogle Scholar
  41. Finlayson SA, Hays DB, Morgan PW (2007) phyB-1 sorghum maintains responsiveness to simulated shade, irradiance and red light : far-red light. Plant Cell Environ 30:952–962PubMedCrossRefGoogle Scholar
  42. Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621PubMedPubMedCentralCrossRefGoogle Scholar
  43. Folta KM, Pontin MA, Karlin-Neumann G, Bottini R, Spalding EP (2003) Genomic and physiological studies of early cryptochrome 1 action demonstrate roles for auxin and gibberellin in the control of hypocotyl growth by blue light. Plant J 36:203–214PubMedCrossRefGoogle Scholar
  44. Foo E, Ross JJ, Davies NW, Reid JB, Weller JL (2006) A role for ethylene in the phytochrome-mediated control of vegetative development. Plant J 46:911–921PubMedCrossRefGoogle Scholar
  45. Frank MJ, Smith LG (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Biol 12:849–853PubMedCrossRefGoogle Scholar
  46. Fredeen AL, Gamon JA, Field CB (1991) Responses of photosynthesis and carbohydrate-partitioning to limitations in nitrogen and water availability in field-grown sunflower. Plant Cell Environ 14:963–970CrossRefGoogle Scholar
  47. Fu Y, Li H, Yang Z (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777–794PubMedPubMedCentralCrossRefGoogle Scholar
  48. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700PubMedCrossRefGoogle Scholar
  49. Fu Y, Xu T, Zhu L, Wen M, Yang Z (2009) A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol 19:1827–1832PubMedPubMedCentralCrossRefGoogle Scholar
  50. Fujioka S, Li J, Choi YH, Seto H, Takatsuto S, Noguchi T et al (1997) The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell 9:1951–1962PubMedPubMedCentralCrossRefGoogle Scholar
  51. Fujikura U, Horiguchi G, Tsukaya H (2007) Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol 48:278–286PubMedCrossRefPubMedCentralGoogle Scholar
  52. Garnier E (1991) Resource capture, biomass allocation and growth in herbaceous plants. Trends Ecol Evol 6:126–131PubMedCrossRefGoogle Scholar
  53. Garnier E (1992) Growth analysis of congeneric annual and perennial grass species. J Ecol 80:665–675CrossRefGoogle Scholar
  54. Giovane A, Balestrieri C, Quagliuolo L, Castaldo D, Servillo L (1995) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit. Purification by affinity chromatography and evidence of a ripening-related precursor. Eur J Biochem 233:926–929PubMedCrossRefGoogle Scholar
  55. Gommers CMM, Visser EJW, Onge KRS, Voesenek LACJ, Pierik R (2013) Shade tolerance: when growing tall is not an option. Trends Plant Sci 18:65–71PubMedCrossRefGoogle Scholar
  56. Graham LE, Graham JM, Wilcox LW (2006) Plant biology. Pearson Prentice Hall, New JerseyGoogle Scholar
  57. Guerriero G, Hausman JF, Cai G (2014) No stress! Relax! Mechanisms governing growth and shape in plant cells. Int J Mol Sci 15:5094–5114PubMedPubMedCentralCrossRefGoogle Scholar
  58. Han Y, Wang W, Sun J, Ding M, Zhao R, Deng S et al (2013) Populus euphratica XTH overexpression enhances salinity tolerance by the development of leaf succulence in transgenic tobacco plants. J Exp Bot 64:4225–4238PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hara Y, Yokoyama R, Osakabe K, Toki S, Nishitani K (2014) Function of xyloglucan endotransglucosylase/hydrolases in rice. Ann Bot 114:1309–1318PubMedCrossRefGoogle Scholar
  60. Havko N, Major I, Jewell J, Attaran E, Browse J, Howe G (2016) Carbon assimilation and partitioning by jasmonate: an accounting of growth–defense tradeoffs. Plants 5:7PubMedCentralCrossRefPubMedGoogle Scholar
  61. Heldt H-W, Piechulla B (2010) Plant Biochemistry. Academic, LondonGoogle Scholar
  62. Held MA, Penning B, Brandt AS, Kessans SA, Yong W, Scofield SR, Carpita NC (2008) Small-interfering RNAs from natural antisense transcripts derived from a cellulose synthase gene modulate cell wall biosynthesis in barley. Proc Natl Acad Sci U S A 105:20534–20539PubMedPubMedCentralCrossRefGoogle Scholar
  63. Held MA, Be E, Zemelis S, Withers S, Wilkerson C, Brandizzi F (2011) CGR3: a Golgi-localized protein influencing homogalacturonan methylesterification. Mol Plant 4:832–844PubMedCrossRefGoogle Scholar
  64. Hirose F, Inagaki N, Hanada A, Yamaguchi S, Kamiya Y, Miyao A et al (2012) Cryptochrome and phytochrome cooperatively but independently reduce active gibberellin content in rice seedlings under light irradiation. Plant Cell Physiol 53:1570–1582PubMedPubMedCentralCrossRefGoogle Scholar
  65. Hisamatsu T, King RW, Helliwell CA, Koshioka M (2005) The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis. Plant Physiol 138:1106–1116PubMedPubMedCentralCrossRefGoogle Scholar
  66. Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1324PubMedPubMedCentralCrossRefGoogle Scholar
  67. Honda H, Fisher JB (1978) Tree branch angle: maximizing effective leaf area. Science 199:888–890PubMedCrossRefGoogle Scholar
  68. Hou X, Lee LY, Xia K, Yan Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884–894PubMedCrossRefGoogle Scholar
  69. Hu L, Millet DB, Mohr MJ, Wells KC, Griffis TJ, Helmig D (2011) Sources and seasonality of atmospheric methanol based on tall tower measurements in the US Upper Midwest. Atmos Chem Phys 11:11145–11156CrossRefGoogle Scholar
  70. Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70PubMedPubMedCentralCrossRefGoogle Scholar
  71. Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645PubMedPubMedCentralCrossRefGoogle Scholar
  72. Jan A, Yang G, Nakamura H, Ichikawa H, Kitano H, Matsuoka M et al (2004) Characterization of a xyloglucan endotransglucosylase gene that is up-regulated by gibberellin in rice. Plant Physiol 136:3670–3681PubMedPubMedCentralCrossRefGoogle Scholar
  73. Jiang CM, Li CP, Chang JC, Chang HM (2002) Characterization of pectinesterase inhibitor in jelly fig (Ficus awkeotsang Makino) achenes. J Agric Food Chem 50:4890–4894PubMedCrossRefGoogle Scholar
  74. Kalve S, Fotschki J, Beeckman T, Vissenberg K, Beemster GTS (2014) Three-dimensional patterns of cell division and expansion throughout the development of Arabidopsis thaliana leaves. J Exp Bot 65(22):6385–6397PubMedCrossRefGoogle Scholar
  75. Karve AA, Jawdy SS, Gunter LE, Allen SM, Yang X, Tuskan GA et al (2012) Initial characterization of shade avoidance response suggests functional diversity between Populus phytochrome B genes. New Phytol 196:726–737PubMedCrossRefGoogle Scholar
  76. Kawade K, Horiguchi G, Usami T, Hirai Masami Y, Tsukaya H (2013) ANGUSTIFOLIA3 signaling coordinates proliferation between clonally distinct cells in leaves. Curr Biol 23:788–792PubMedCrossRefGoogle Scholar
  77. Keuskamp DH, Sasidharan R, Vos I, Peeters AJ, Voesenek LA, Pierik R (2011) Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. Plant J 67:208–217PubMedCrossRefGoogle Scholar
  78. Kim G-T, Tsukaya H, Uchimiya H (1998) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev 12:2381–2391PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kim GT, Shoda K, Tsuge T, Cho KH, Uchimiya H, Yokoyama R et al (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J 21:1267–1279PubMedPubMedCentralCrossRefGoogle Scholar
  80. Kim G-T, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S, Tsukaya H (2005) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 41:710–721PubMedCrossRefGoogle Scholar
  81. Kim G-T, Cho K-H (2006) Recent advances in the genetic regulation of the shape of simple leaves. Physiol Plant 126:494–502Google Scholar
  82. Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–376PubMedCrossRefGoogle Scholar
  83. Kim S-J, Held MA, Zemelis S, Wilkerson C, Brandizzi F (2015) CGR2 and CGR3 have critical overlapping roles in pectin methylesterification and plant growth in Arabidopsis thaliana. Plant J 82:208–220PubMedCrossRefGoogle Scholar
  84. Kost B (2010) Regulatory and cellular functions of plant RhoGAPs and RhoGDIs. In: Yalovsky S, Baluška F, Jones A (eds) Integrated G Proteins Signaling in Plants. Springer, Berlin/Heidelberg, pp 27–48CrossRefGoogle Scholar
  85. Kozuka T, Horiguchi G, Kim GT, Ohgishi M, Sakai T, Tsukaya H (2005) 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 46:213–223PubMedCrossRefGoogle Scholar
  86. Krupkova E, Immerzeel P, Pauly M, Schmulling T (2007) The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant DEVELOPMENT. Plant J 50:735–750PubMedCrossRefGoogle Scholar
  87. Lambers H, Chapin F, Pons T (2008) Plant physiological ecology. Springer, NewYorkCrossRefGoogle Scholar
  88. Leduc N, Roman H, Barbier F, Péron T, Huché-Thélier L, Lothier J et al (2014) Light signaling in bud outgrowth and branching in plants. Plants 3:223PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lee CM, Thomashow MF (2012) Photoperiodic regulation of the C–repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci U S A 109:15054–15059PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lee YK, Kim GT, Kim IJ, Park J, Kwak SS, Choi G, Chung WI (2006) LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development 133:4305–4314PubMedCrossRefGoogle Scholar
  91. Levesque-Tremblay G, Muller K, Mansfield SD, Haughn GW (2015) HIGHLY METHYL ESTERIFIED SEEDS is a pectin methyl esterase involved in embryo development. Plant Physiol 167:725–737PubMedPubMedCentralCrossRefGoogle Scholar
  92. Li S, Blanchoin L, Yang Z, Lord EM (2003) The putative Arabidopsis arp2/3 complex controls leaf cell morphogenesis. Plant Physiol 132:2034–2044PubMedPubMedCentralCrossRefGoogle Scholar
  93. Li Y, Sorefan K, Hemmann G, Bevan MW (2004) Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiol 136:3616–3627PubMedPubMedCentralCrossRefGoogle Scholar
  94. Lionetti V, Raiola A, Camardella L, Giovane A, Obel N, Pauly M et al (2007) Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol 143:1871–1880PubMedPubMedCentralCrossRefGoogle Scholar
  95. Liu YB, Lu SM, Zhang JF, Liu S, Lu YT (2007) A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis. Planta 226:1547–1560PubMedCrossRefGoogle Scholar
  96. Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ et al (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952PubMedCrossRefGoogle Scholar
  97. Marcotrigiano M (2010) A role for leaf epidermis in the control of leaf size and the rate and extent of mesophyll cell division. Am J Bot 97:224–233PubMedCrossRefGoogle Scholar
  98. Markovic O, Janecek S (2004) Pectin methylesterases: sequence-structural features and phylogenetic relationships. Carbohydr Res 339:2281–2295PubMedCrossRefGoogle Scholar
  99. Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436:866–870PubMedCrossRefGoogle Scholar
  100. Mathur J (2006) Local interactions shape plant cells. Curr Opin Cell Biol 18:40–46PubMedCrossRefGoogle Scholar
  101. Mathur J, Hülskamp M (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Curr Biol 12:R669–R676PubMedCrossRefGoogle Scholar
  102. Matsui A, Yokoyama R, Seki M, Ito T, Shinozaki K, Takahashi T et al (2005) AtXTH27 plays an essential role in cell wall modification during the development of tracheary elements. Plant J 42:525–534PubMedCrossRefGoogle Scholar
  103. Mazzella MA, Casal JJ, Muschietti JP, Fox AR (2014) Hormonal networks involved in apical hook development in darkness and their response to light. Front Plant Sci 5:52PubMedPubMedCentralCrossRefGoogle Scholar
  104. Miao Y, Li HY, Shen J, Wang J, Jiang L (2011) QUASIMODO 3 (QUA3) is a putative homogalacturonan methyltransferase regulating cell wall biosynthesis in Arabidopsis suspension-cultured cells. J Exp Bot 62:5063–5078PubMedPubMedCentralCrossRefGoogle Scholar
  105. Milla-Moreno EA, McKown AD, Guy RD, Soolanayakanahally RY (2016) Leaf mass per area predicts palisade structural properties linked to mesophyll conductance in balsam poplar (Populus balsamifera L.). Botany 94:225–239CrossRefGoogle Scholar
  106. Miura K, Hasegawa PM (2010) Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20:223–232PubMedCrossRefGoogle Scholar
  107. Monsi M (1960) Dry-matter reproduction in plants 1. Schemata of dry-matter reproduction. Bot Mag Tokyo 73:81–90CrossRefGoogle Scholar
  108. Moon SY, Zheng Y (2003) Rho GTPase-activating proteins in cell regulation. Trends Cell Biol 13:13–22PubMedCrossRefGoogle Scholar
  109. Mouille G, Ralet MC, Cavelier C, Eland C, Effroy D, Hematy K et al (2007) Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J 50:605–614PubMedCrossRefGoogle Scholar
  110. Müller K, Levesque-Tremblay G, Bartels S, Weitbrecht K, Wormit A, Usadel B et al (2013a) Demethylesterification of cell wall pectins in Arabidopsis plays a role in seed germination. Plant Physiol 161:305–316PubMedCrossRefGoogle Scholar
  111. Müller K, Levesque-Tremblay G, Fernandes A, Wormit A, Bartels S, Usadel B, Kermode A (2013b) Overexpression of a pectin methylesterase inhibitor in Arabidopsis thaliana leads to altered growth morphology of the stem and defective organ separation. Plant Signal Behav 8:e26464PubMedPubMedCentralCrossRefGoogle Scholar
  112. Nagel OW, Konings H, Lambers H (2001) Growth rate and biomass partitioning of wildtype and low-gibberellin tomato (Solanum lycopersicum) plants growing at a high and low nitrogen supply. Physiol Plant 111:33–39CrossRefGoogle Scholar
  113. Nakaya M, Tsukaya H, Murakami N, Kato M (2002) Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant Cell Physiol 43:239–244PubMedCrossRefGoogle Scholar
  114. Neumetzler L, Humphrey T, Lumba S, Snyder S, Yeats TH, Usadel B et al (2012) The FRIABLE1 gene product affects cell adhesion in Arabidopsis. PLoS One 7:14CrossRefGoogle Scholar
  115. Niinemets Ü (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469CrossRefGoogle Scholar
  116. Nishitani K, Tominaga R (1992) Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem 267:21058–21064PubMedGoogle Scholar
  117. Ochoa-Villarreal M, Aispuro-Hernández E, Vargas-Arispuro I, Martínez-Téllez MÁ (2012) Plant cell wall polymers: function, structure and biological activity of their derivatives. In: De Souza Gomes A (ed) Polymerization. InTech, Rijeka. Available from: CrossRefGoogle Scholar
  118. Ogawa S, Toyomasu T, Yamane H, Murofushi N, Ikeda R, Morimoto Y et al (1996) A step in the biosynthesis of gibberellins that is controlled by the mutation in the semi-dwarf rice cultivar tan-ginbozu. Plant Cell Physiol 37:363–368CrossRefGoogle Scholar
  119. Ohnishi T, Szatmari AM, Watanabe B, Fujita S, Bancos S, Koncz C et al (2006) C-23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell 18:3275–3288PubMedPubMedCentralCrossRefGoogle Scholar
  120. Oikawa PY, Giebel BM, Sternberg Lda S, Li L, Timko MP, Swart PK et al (2011) Leaf and root pectin methylesterase activity and 13C/12C stable isotopic ratio measurements of methanol emissions give insight into methanol production in Lycopersicon esculentum. New Phytol 191:1031–1040PubMedCrossRefGoogle Scholar
  121. Orfila C, Seymour GB, Willats WG, Huxham IM, Jarvis MC, Dover CJ et al (2001) Altered middle lamella homogalacturonan and disrupted deposition of (1-->5)-α-L-arabinan in the pericarp of Cnr, a ripening mutant of tomato. Plant Physiol 126:210–221PubMedPubMedCentralCrossRefGoogle Scholar
  122. Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci U S A 93:12637–12642PubMedPubMedCentralCrossRefGoogle Scholar
  123. Peaucelle A, Louvet R, Johansen JN, Hofte H, Laufs P, Pelloux J, Mouille G (2008) Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr Biol 18:1943–1948PubMedCrossRefGoogle Scholar
  124. Peaucelle A, Braybrook S, Hofte H (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3:121PubMedPubMedCentralCrossRefGoogle Scholar
  125. Pierik R, De Wit M, Voesenek LA (2011) Growth-mediated stress escape: convergence of signal transduction pathways activated upon exposure to two different environmental stresses. New Phytol 189:122–134PubMedCrossRefGoogle Scholar
  126. Pilling J, Willmitzer L, Bucking H, Fisahn J (2004) Inhibition of a ubiquitously expressed pectin methyl esterase in Solanum tuberosum L. affects plant growth, leaf growth polarity, and ion partitioning. Planta 219:32–40PubMedCrossRefGoogle Scholar
  127. Poorter H, Lambers H (1991) Is interspecific variation in relative growth rate positively correlated with biomass allocation to the leaves? Am Nat 138:1264–1268CrossRefGoogle Scholar
  128. Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83:553–559PubMedCrossRefGoogle Scholar
  129. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588PubMedCrossRefGoogle Scholar
  130. Qian P, Hou S, Guo G (2009) Molecular mechanisms controlling pavement cell shape in Arabidopsis leaves. Plant Cell Rep 28:1147–1157PubMedCrossRefGoogle Scholar
  131. Qiu JL, Jilk R, Marks MD, Szymanski DB (2002) The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14:101–118PubMedPubMedCentralCrossRefGoogle Scholar
  132. Raiola A, Camardella L, Giovane A, Mattei B, De Lorenzo G, Cervone F, Bellincampi D (2004) Two Arabidopsis thaliana genes encode functional pectin methylesterase inhibitors. FEBS Lett 557:199–203PubMedCrossRefGoogle Scholar
  133. Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G et al (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant-Microbe Interact 24:432–440PubMedCrossRefGoogle Scholar
  134. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5:147–157PubMedPubMedCentralCrossRefGoogle Scholar
  135. Robert S, Mouille G, Höfte H (2004) The mechanism and regulation of cellulose synthesis in primary walls: lessons from cellulose-deficient Arabidopsis mutants. Cellulose 11:351–364CrossRefGoogle Scholar
  136. Rose JK, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435PubMedCrossRefGoogle Scholar
  137. Sánchez-Rodríguez C, Estévez JM, Llorente F, Hernández-Blanco C, Jordá L, Pagán I et al (2009) The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in Arabidopsis thaliana. Mol Plant-Microbe Interact 22:953–963PubMedCrossRefGoogle Scholar
  138. Savaldi-Goldstein S, Chory J (2008) Growth coordination and the shoot epidermis. Curr Opin Plant Biol 11:42–48PubMedCrossRefGoogle Scholar
  139. Shin YK, Yum H, Kim ES, Cho H, Gothandam KM, Hyun J, Chung YY (2006) BcXTH1, a Brassica campestris homologue of Arabidopsis XTH9, is associated with cell expansion. Planta 224:32–41PubMedCrossRefGoogle Scholar
  140. Shipley B (2002) Trade-offs between net assimilation rate and specific leaf area in determining relative growth rate: relationship with daily irradiance. Funct Ecol 16:682–689CrossRefGoogle Scholar
  141. 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 131:1491–1501PubMedPubMedCentralCrossRefGoogle Scholar
  142. Sinha N (1999) Leaf development in angiosperms. Annu Rev Plant Physiol Plant Mol Biol 50:419–446PubMedCrossRefGoogle Scholar
  143. Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR (2009) Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant Cell Environ 32:1821–1832PubMedCrossRefPubMedCentralGoogle Scholar
  144. Suzuki S, Li L, Sun YH, Chiang VL (2006) The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol 142:1233–1245PubMedPubMedCentralCrossRefGoogle Scholar
  145. Tan H-T, Shirley NJ, Singh RR, Henderson M, Dhugga KS, Mayo GM et al (2015) Powerful regulatory systems and post-transcriptional gene silencing resist increases in cellulose content in cell walls of barley. BMC Plant Biol 15:62PubMedPubMedCentralCrossRefGoogle Scholar
  146. Tenhaken R (2015) Cell wall remodeling under abiotic stress. Front Plant Sci 5:771PubMedPubMedCentralCrossRefGoogle Scholar
  147. Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57:343–354PubMedCrossRefPubMedCentralGoogle Scholar
  148. Tillman D (1991) Relative growth rates and plant allocation patterns. Am Nat 138:1269–1275CrossRefGoogle Scholar
  149. Tosens T, Niinemets Ü, Vislap V, Eichelmann H, Castro Díez P (2012) Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function. Plant Cell Environ 35:839–856PubMedCrossRefGoogle Scholar
  150. Tsuge T, Tsukaya H, Uchimiya H (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L). Heynh Development 122:1589–1600PubMedGoogle Scholar
  151. Tsukaya H (1998) Genetic evidence for polarities that regulate leaf morphogenesis. J Plant Res 111:113–119CrossRefGoogle Scholar
  152. Tsukaya H (2002) The leaf index: heteroblasty, natural variation, and the genetic control of polar processes of leaf expansion. Plant Cell Physiol 43:372–378PubMedCrossRefGoogle Scholar
  153. Tsukaya H, Kozuka T, Kim G-T (2002) Genetic control of petiole length in Arabidopsis thaliana. Plant Cell Physiol 43:1221–1228PubMedCrossRefGoogle Scholar
  154. Utrillas MJ, Alegre L (1997) Impact of water stress on leaf anatomy and ultrastructure in Cynodon dactylon (L.) Pers. under natural conditions. Int J Plant Sci 158:313–324CrossRefGoogle Scholar
  155. Van Volkenburgh E, Boyer JS (1985) Inhibitory effects of water deficit on maize leaf elongation. Plant Physiol 77:190–194PubMedPubMedCentralCrossRefGoogle Scholar
  156. Verica JA, Medford JI (1997) Modified MER15 expression alters cell expansion in transgenic Arabidopsis plants. Plant Sci 125:201–210CrossRefGoogle Scholar
  157. Villagarcia H, Morin A-C, Shpak ED, Khodakovskaya MV (2012) Modification of tomato growth by expression of truncated ERECTA protein from Arabidopsis thaliana. J Exp Bot 63:6493–6504PubMedCrossRefGoogle Scholar
  158. Villar R, Ruiz-Robleto J, Ubera JL, Poorter H (2013) Exploring variation in leaf mass per area (LMA) from leaf to cell: an anatomical analysis of 26 woody species. Am J Bot 100:1969–1980PubMedCrossRefGoogle Scholar
  159. Volpi C, Janni M, Lionetti V, Bellincampi D, Favaron F, D’Ovidio R (2011) The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant-Microbe Interact 24:1012–1019PubMedCrossRefGoogle Scholar
  160. Wang X, Zhang J, Yuan M, Ehrhardt DW, Wang Z, Mao T (2012) Arabidopsis microtubule destabilizing protein40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24:4012–4025PubMedPubMedCentralCrossRefGoogle Scholar
  161. Weller JL, Hecht V, Vander Schoor JK, Davidson SE, Ross JJ (2009) Light regulation of gibberellin biosynthesis in pea is mediated through the COP1/HY5 pathway. Plant Cell 21:800–813PubMedPubMedCentralCrossRefGoogle Scholar
  162. Weraduwage S, Chen J, Anozie FC, Morales A, Weise SE, Sharkey TD (2015) The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana. Front Plant Sci 6:167PubMedPubMedCentralCrossRefGoogle Scholar
  163. Weraduwage SM, Kim S-J, Renna L, Anozie FC, Sharkey TD, Brandizzi F (2016) Pectin methylesterification impacts the relationship between photosynthesis and plant growth in Arabidopsis thaliana. Plant Physiol 171:833–848Google Scholar
  164. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610–613PubMedCrossRefGoogle Scholar
  165. Wietholter N, Graessner B, Mierau M, Mort AJ, Moerschbacher BM (2003) Differences in the methyl ester distribution of homogalacturonans from near-isogenic wheat lines resistant and susceptible to the wheat stem rust fungus. Mol Plant-Microbe Interact 16:945–952PubMedCrossRefGoogle Scholar
  166. Williamson RE, Burn JE, Birch R, Baskin TI, Arioli T, Betzner AS, Cork A (2001) Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma 215:116–127PubMedCrossRefGoogle Scholar
  167. Wood PJ, Siddiqui IR (1971) Determination of methanol and its application to measurement of pectin ester content and pectin methylesterase activity. Anal Biochem 39:418–428PubMedCrossRefGoogle Scholar
  168. Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851–860PubMedCrossRefGoogle Scholar
  169. Xiao C, Anderson CT (2013) Roles of pectin in biomass yield and processing for biofuels. Front Plant Sci 4:67PubMedPubMedCentralCrossRefGoogle Scholar
  170. Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ et al (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110PubMedPubMedCentralCrossRefGoogle Scholar
  171. Yang Y, Karlson D (2012) Effects of mutations in the Arabidopsis cold shock domain protein 3 (AtCSP3) gene on leaf cell expansion. J Exp Bot 63:4861–4873PubMedPubMedCentralCrossRefGoogle Scholar
  172. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q et al (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci U S A 109:E1192–E1200PubMedPubMedCentralCrossRefGoogle Scholar
  173. Yokoyama R, Nishitani K (2001) A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant Cell Physiol 42:1025–1033PubMedCrossRefGoogle Scholar
  174. Yokoyama R, Rose JK, Nishitani K (2004) A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis. Plant Physiol 134:1088–1099PubMedPubMedCentralCrossRefGoogle Scholar
  175. Yoshikawa T, Eiguchi M, Hibara K-I, Ito J-I, Nagato Y (2013) Rice SLENDER LEAF 1 gene encodes cellulose synthase-like D4 and is specifically expressed in M-phase cells to regulate cell proliferation. J Exp Bot 64:2049–2061PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Sarathi M. Weraduwage
    • 1
    • 2
  • Marcelo L. Campos
    • 1
    • 3
  • Yuki Yoshida
    • 1
    • 4
  • Ian T. Major
    • 1
  • Yong-Sig Kim
    • 1
  • Sang-Jin Kim
    • 1
    • 5
  • Luciana Renna
    • 1
    • 5
  • Fransisca C. Anozie
    • 6
  • Federica Brandizzi
    • 1
    • 7
    • 8
    • 9
  • Michael F. Thomashow
    • 1
    • 8
    • 9
    • 2
  • Gregg A. Howe
    • 1
    • 6
    • 2
  • Thomas D. Sharkey
    • 1
    • 5
    • 6
    • 2
    Email author
  1. 1.MSU-DOE Plant Research LaboratoryMichigan State UniversityEast LansingUSA
  2. 2.Plant Resilience InstituteMichigan State UniversityEast LansingUSA
  3. 3.Departamento de Botânica, Instituto de Ciências BiológicasUniversidade de BrasíliaBrasíliaBrazil
  4. 4.Graduate School of ScienceThe University of TokyoTokyoJapan
  5. 5.DOE Great Lakes Bioenergy Research CenterMichigan State UniversityEast LansingUSA
  6. 6.Department of Biochemistry and Molecular BiologyMichigan State UniversityEast LansingUSA
  7. 7.Department of Plant BiologyMichigan State UniversityEast LansingUSA
  8. 8.Department of Plant, Soil and Microbial SciencesMichigan State UniversityEast LansingUSA
  9. 9.Department of Microbiology and Molecular GeneticsMichigan State UniversityEast LansingUSA

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