Spatio-temporal orientation of microtubules controls conical cell shape in Arabidopsis thaliana petals

PLoS Genet. 2017 Jun 23;13(6):e1006851. doi: 10.1371/journal.pgen.1006851. eCollection 2017 Jun.

Abstract

The physiological functions of epidermal cells are largely determined by their diverse morphologies. Most flowering plants have special conical-shaped petal epidermal cells that are thought to influence light capture and reflectance, and provide pollinator grips, but the molecular mechanisms controlling conical cell shape remain largely unknown. Here, we developed a live-confocal imaging approach to quantify geometric parameters of conical cells in Arabidopsis thaliana (A. thaliana). Through genetic screens, we identified katanin (KTN1) mutants showing a phenotype of decreased tip sharpening of conical cells. Furthermore, we demonstrated that SPIKE1 and Rho of Plants (ROP) GTPases were required for the final shape formation of conical cells, as KTN1 does. Live-cell imaging showed that wild-type cells exhibited random orientation of cortical microtubule arrays at early developmental stages but displayed a well-ordered circumferential orientation of microtubule arrays at later stages. By contrast, loss of KTN1 prevented random microtubule networks from shifting into well-ordered arrays. We further showed that the filamentous actin cap, which is a typical feature of several plant epidermal cell types including root hairs and leaf trichomes, was not observed in the growth apexes of conical cells during cell development. Moreover, our genetic and pharmacological data suggested that microtubules but not actin are required for conical cell shaping. Together, our results provide a novel imaging approach for studying petal conical cell morphogenesis and suggest that the spatio-temporal organization of microtubule arrays plays crucial roles in controlling conical cell shape.

MeSH terms

  • Actin Cytoskeleton / genetics
  • Adenosine Triphosphatases / genetics*
  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis Proteins / genetics*
  • Cell Shape / genetics*
  • Epidermal Cells
  • Epidermis / growth & development
  • Flowers / genetics*
  • Flowers / growth & development
  • Flowers / ultrastructure
  • GTP-Binding Proteins / genetics
  • Katanin
  • Microtubules / genetics
  • Microtubules / ultrastructure
  • Mutant Proteins / genetics
  • Plant Leaves / cytology
  • Plant Leaves / genetics
  • Trichomes / genetics
  • Trichomes / ultrastructure

Substances

  • Arabidopsis Proteins
  • Mutant Proteins
  • SPIKE1 protein, Arabidopsis
  • Adenosine Triphosphatases
  • GTP-Binding Proteins
  • ROP1 protein, Arabidopsis
  • KTN1 protein, Arabidopsis
  • Katanin

Grants and funding

This work was supported by the National Natural Science Foundation of China (http://www.nsfc.gov.cn) (Grant 31500160) to HR and (Grant 31570278) to DL, and the Natural Science Foundation of Fujian Province (http://www.fjkjt.gov.cn/) (Grant 2016J06007) to DL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.