Ultrastructure and development of non-contiguous stomatal clusters and helicocytic patterning in Begonia

Paula J Rudall, Adele C M Julier, Catherine A Kidner

Research output: Contribution to journalArticlepeer-review

Abstract

Background and Aims: Helicocytic stomata are characterized by an inward spiral of mesogenous cells surrounding a central stomatal pore. They represent a relatively rare feature that occurs in some drought-tolerant angiosperm species. In some Begonia species with thick leaves, the stomata are not only helicocytic but also clustered into groups that are spaced apart by at least one cell. This paper presents a detailed ontogenetic study of this characteristic non-contiguous stomatal patterning in a developmental and phylogenetic context.

Methods: Light microscopy and both scanning and transmission electron microscopy were used to examine stomatal development in several species of Begonia. Published reports of stomatal development in Begonia and other angiosperms were reviewed to provide a comprehensive discussion of the evolution of stomatal patterning.

Key Results: Helicocytic stomata develop from meristemoids that undergo a series of oriented asymmetric divisions to produce a spiral of mesogene stomatal lineage ground cells (SLGCs) surrounding a stoma. A clear developmental similarity between anisocytic and helicocytic stomata is positively correlated with the number of iterations of amplifying divisions that result in SLGCs. Stomatal clusters develop from asymmetric divisions in neighbouring SLGCs. Within each cluster, non-contiguous spacing of meristemoids is maintained by asymmetric divisions oriented away from each developing meristemoid.

Conclusions: Formation of non-contiguous stomatal clusters in Begonia relies on two primary developmental factors in the epidermis: an inwardly spiralling series of amplifying divisions that result in helicocytic stomata, and the development of a variable number of meristemoids from neighbouring SLGCs within each cluster. Optimization of these features on an angiosperm phylogeny indicates that the occurrence of amplifying divisions could be pre-adaptive for these factors. Both factors have been thoroughly studied in terms of developmental genetics in Arabidopsis, suggesting gene orthologues that could be implicated in Begonia stomatal patterning.

Original languageEnglish
Pages (from-to)767-776
Number of pages17
JournalAnnals of Botany
Volume122
Issue number5
Early online date23 Nov 2017
DOIs
Publication statusPublished - 5 Oct 2018

Keywords

  • amplifying divisions
  • anisoocytic stomata
  • helicocytic stomata
  • Begonia
  • meristemoids
  • non-contiguous stomatal clusters
  • stomatal development

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