Hypothesis & Theory ARTICLE

Front. Plant Sci., 12 October 2011 | doi: 10.3389/fpls.2011.00062

Geometric constraints and the anatomical interpretation of twisted plant organ phenotypes

  • 1 Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, USA
  • 2 Department of Biology, Indiana/Purdue University Fort Wayne, Fort Wayne, IN, USA

The study of plant mutants with twisting growth in axial organs, which normally grow straight in the wild-type, is expected to improve our understanding of the interplay among microtubules, cellulose biosynthesis, cell wall structure, and organ biomechanics that control organ growth and morphogenesis. However, geometric constraints based on symplastic growth and the consequences of these geometric constraints concerning interpretations of twisted-organ phenotypes are currently underestimated. Symplastic growth, a fundamental concept in plant developmental biology, is characterized by coordinated growth of adjacent cells based on their connectivity through cell walls. This growth behavior implies that in twisting axial organs, all cell files rotate in phase around the organ axis, as has been illustrated for the Arabidopsis spr1 and twd1 mutants in this work. Evaluating the geometry of such organs, we demonstrate that a radial gradient in cell elongation and changes in cellular growth anisotropy must occur in twisting organs out of geometric necessity alone. In-phase rotation of the different cell layers results in a decrease of length and angle toward organ axis from the outer cell layers inward. Additionally, the circumference of each cell layer increases in twisting organs, which requires compensation through radial expansion or an adjustment of cell number. Therefore, differential cell elongation and growth anisotropy cannot serve as arguments for or against specific hypotheses regarding the molecular cause of twisting growth. We suggest instead, that based on mathematical modeling, geometric constraints in twisting organs are indispensable for the explanation of the causal connection of molecular and biomechanical processes in twisting as well as normal organs.

Keywords: Arabidopsis thaliana, developmental biomechanics, spiral1 (spr1) mutant, symplastic growth, tissue geometry, tissue tension, twisted dwarf1 (twd1) mutant, twisting growth

Citation: Weizbauer R, Peters WS and Schulz B (2011) Geometric constraints and the anatomical interpretation of twisted plant organ phenotypes. Front. Plant Sci. 2:62. doi: 10.3389/fpls.2011.00062

Received: 29 June 2011; Accepted: 14 September 2011;
Published online: 13 October 2011.

Edited by:

Jan Traas, UMR INRA–CNRS–ENSL–UCBL, France

Reviewed by:

Gabriel Krouk, CNRS, France
Arezki Boudaoud, Ecole Normale Supérieure de Lyon, France

Copyright: © 2011 Weizbauer, Peters and Schulz. This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

*Correspondence: Burkhard Schulz, Department of Horticulture and Landscape Architecture, Purdue University, 625 Agriculture Mall Drive, West Lafayette, IN 47907, USA. e-mail: bschulz@purdue.edu

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