Reactive oxygen species mediate conical cell shaping in Arabidopsis thaliana petals

PLoS Genet. 2018 Oct 8;14(10):e1007705. doi: 10.1371/journal.pgen.1007705. eCollection 2018 Oct.

Abstract

Plants have evolved diverse cell types with distinct sizes, shapes, and functions. For example, most flowering plants contain specialized petal conical epidermal cells that are thought to attract pollinators and influence light capture and reflectance, but the molecular mechanisms controlling conical cell shaping remain unclear. Here, through a genetic screen in Arabidopsis thaliana, we demonstrated that loss-of-function mutations in ANGUSTIFOLIA (AN), which encodes for a homolog of mammalian CtBP/BARs, displayed conical cells phenotype with wider tip angles, correlating with increased accumulation of reactive oxygen species (ROS). We further showed that exogenously supplied ROS generated similar conical cell phenotypes as the an mutants. Moreover, reduced endogenous ROS levels resulted in deceased tip sharpening of conical cells. Furthermore, through enhancer screening, we demonstrated that mutations in katanin (KTN1) enhanced conical cell phenotypes of the an-t1 mutants. Genetic analyses showed that AN acted in parallel with KTN1 to control conical cell shaping. Both increased or decreased ROS levels and mutations in AN suppressed microtubule organization into well-ordered circumferential arrays. We demonstrated that the AN-ROS pathway jointly functioned with KTN1 to modulate microtubule ordering, correlating with the tip sharpening of conical cells. Collectively, our findings revealed a mechanistic insight into ROS homeostasis regulation of microtubule organization and conical cell shaping.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / cytology*
  • Arabidopsis / physiology
  • Arabidopsis Proteins / genetics*
  • Cell Shape / physiology*
  • Epidermal Cells / metabolism
  • Epidermis / metabolism
  • Flowers / genetics
  • Flowers / metabolism
  • Katanin / genetics
  • Microtubules / genetics
  • Reactive Oxygen Species / metabolism
  • Repressor Proteins / genetics*

Substances

  • ANGUSTIFOLIA protein, Arabidopsis
  • Arabidopsis Proteins
  • Reactive Oxygen Species
  • Repressor Proteins
  • KTN1 protein, Arabidopsis
  • Katanin

Grants and funding

This work was supported by the National Natural Science Foundation of China (http://www.nsfc.gov.cn) (Grants 31570278 and 31771344) to DL and (Grant 31500160) to HR, the Natural Science Foundation of Fujian Province (http://www.fjkjt.gov.cn/) (Grant 2016J06007) to DL. XD is supported by the Scientific Research Foundation of Graduate School of Fujian Agriculture and Forestry University (324-1122yb040) and the project of “Excellent initiative” for graduate students of College of Life Science (http://skxy.fafu.edu.cn), Fujian Agriculture and Forestry University. DL is partly supported by the open funding of State Key Laboratory of Plant Physiology and Biochemistry, China Agricultural University(http://www.cau.edu.cn). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.