Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 23, 2014, Pages 8685-8690

  Bassel, George W ^a   Stamm, Petra ^a   Mosca, Gabriella ^b   De Reuille, Pierre Barbier ^b   Gibbs, Daniel J ^a   Winter, Robin ^c   Janka, Ales ^d   Holdsworth, Michael J ^e   Smith, Richard S ^b,f  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF BERN   (Switzerland)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d Ecole d'Ingenieurs et d'Architectes de Fribourg   (Switzerland)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^f MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

Biomechanics; Computational modeling; Plant development; Quantification; Seed germination

Indexed keywords

GIBBERELLIC ACID;

ARABIDOPSIS; ARTICLE; BIOMECHANICS; BRANCHING MORPHOGENESIS; CELL EXPANSION; CELL GROWTH; CELL SIZE; CYTOARCHITECTURE; EMBRYO PATTERN FORMATION; GENE EXPRESSION; GENE FUNCTION; GERMINATION; NONHUMAN; PLANT CELL; PLANT DEVELOPMENT; PLANT GENE; PLANT GROWTH; PLANT TISSUE; PRIORITY JOURNAL; SIMULATION;

BIOMECHANICS; COMPUTATIONAL MODELING; PLANT DEVELOPMENT; QUANTIFICATION; SEED GERMINATION;

ALGORITHMS; ARABIDOPSIS; CELL SHAPE; CELL SIZE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GERMINATION; GIBBERELLINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED; SEEDS; STRESS, MECHANICAL;

EID: 84902191977     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1404616111     Document Type: Article

References (40)

1. Kennaway R, Coen E, Green A, Bangham A (2011) Generation of diverse biological forms through combinatorial interactions between tissue polarity and growth. PLoS Comput Biol 7(6):e1002071.
2. Coen E, Rolland-Lagan AG, Matthews M, Bangham JA, Prusinkiewicz P (2004) The genetics of geometry. Proc Natl Acad Sci USA 101(14):4728-4735. (Pubitemid 38469146)
3. Kuchen EE, et al. (2012) Generation of leaf shape through early patterns of growth and tissue polarity. Science 335(6072):1092-1096.
4. Green AA, Kennaway JR, Hanna AI, Bangham JA, Coen E (2010) Genetic control of organ shape and tissue polarity. PLoS Biol 8(11):e1000537.
5. Sauret-Güeto S, Schiessl K, Bangham A, Sablowski R, Coen E (2013) JAGGED controls Arabidopsis petal growth and shape by interacting with a divergent polarity field. PLoS Biol 11(4):e1001550.
6. Goriely A, Robertson-Tessi M, Tabor M, Vandiver R (2008) Elastic growth models. Mathematical Modelling of Biosystems, Applied Optimization, eds Mondaini R, Pardalos P (Springer, Berlin), Vol 102, pp 1-44.
7. Lockhart JA (1965) An analysis of irreversible plant cell elongation. J Theor Biol 8(2):264-275.
8. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6(11):850-861.
9. Reinhardt D, Wittwer F, Mandel T, Kuhlemeier C (1998) Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 10(9):1427-1437. (Pubitemid 28542148)
10. Birnbaum K, et al. (2003) A gene expression map of the Arabidopsis root. Science 302(5652):1956-1960. (Pubitemid 37523501)
11. Hamant O, et al. (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322(5908):1650-1655.
12. Weigel D, Jürgens G (2002) Stem cells that make stems. Nature 415(6873):751-754. (Pubitemid 34150488)
13. Yadav RK, et al. (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25(19):2025-2030.
14. Uyttewaal M, et al. (2012) Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149(2):439-451.
15. Schiessl K, Kausika S, Southam P, Bush M, Sablowski R (2012) JAGGED controls growth anisotropy and coordination between cell size and cell cycle during plant organogenesis. Curr Biol 22(19):1739-1746.
16. Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179(1):33-54. (Pubitemid 351783168)
17. Sliwinska E, Bassel GW, Bewley JD (2009) Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyl. J Exp Bot 60(12):3587-3594.
18. Koornneef M, van der Veen JH (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh. Theor Appl Genet 58(6):257-263.
19. Ogawa M, et al. (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15(7):1591-1604. (Pubitemid 36872599)
20. Merks RM, Guravage M, Inzé D, Beemster GT (2011) VirtualLeaf: An open-source framework for cell-based modeling of plant tissue growth and development. Plant Physiol 155(2):656-666.
21. Roeder AHK, et al. (2011) Computational morphodynamics of plants: Integrating development over space and time. Nat Rev Mol Cell Biol 12(4):265-273.
22. Malinowski R, Kasprzewska A, Fleming AJ (2011) Targeted manipulation of leaf form via local growth repression. Plant J 66(6):941-952.
23. Murray JAH, Jones A, Godin C, Traas J (2012) Systems analysis of shoot apical meristem growth and development: Integrating hormonal and mechanical signaling. Plant Cell 24(10):3907-3919.
24. Kierzkowski D, et al. (2012) Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335(6072):1096-1099.
25. Bassel GW, et al. (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 108(23):9709-9714.
26. 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(3):451-467.
27. Plackett ARG, et al. (2012) Analysis of the developmental roles of the Arabidopsis gibberellin 20-oxidases demonstrates that GA20ox1, -2, and -3 are the dominant paralogs. Plant Cell 24(3):941-960.
28. Yamaguchi S, Kamiya Y, Sun T (2001) Distinct cell-specific expression patterns of early and late gibberellin biosynthetic genes during Arabidopsis seed germination. Plant J 28(4):443-453. (Pubitemid 34045591)
29. Sun T, Goodman HM, Ausubel FM (1992) Cloning the Arabidopsis GA1 locus by genomic subtraction. Plant Cell 4(2):119-128.
30. Derbyshire P, Findlay K, McCann MC, Roberts K (2007) Cell elongation in Arabidopsis hypocotyls involves dynamic changes in cell wall thickness. J Exp Bot 58(8):2079-2089. (Pubitemid 47216569)
31. Caderas D, et al. (2000) Limited correlation between expansin gene expression and elongation growth rate. Plant Physiol 123(4):1399-1414.
32. Goh HH, Sloan J, Dorca-Fornell C, Fleming A (2012) Inducible repression of multiple expansin genes leads to growth suppression during leaf development. Plant Physiol 159(4):1759-1770.
33. Rangamani P, et al. (2013) Decoding information in cell shape. Cell 154(6):1356-1369.
34. Truernit E, et al. (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell 20(6):1494-1503. (Pubitemid 352844159)
35. Suzuki H, et al. (2009) Differential expression and affinities of Arabidopsis gibberellin receptors can explain variation in phenotypes of multiple knock-out mutants. Plant J 60(1):48-55.
36. Mitchum MG, et al. (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45(5):804-818. (Pubitemid 43378972)
37. Jang JC, et al. (2000) A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev 14(12):1485-1497.
38. Yatusevich R, et al. (2010) Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J 62(1):1-11.
39. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12(4):507-518. (Pubitemid 30254868)
40. Federl P, Prusinkiewicz P (1999) Virtual Laboratory: An interactive software environment for computer graphics. Proc Comput Graph Int, 93-100.