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Front. Plant Sci. | doi: 10.3389/fpls.2018.01714

Long-distance and trans-generational stomatal patterning by CO2 across Arabidopsis organs

 Miranda J. Haus1, 2*,  Mao Li3, Dan H. Chitwood1 and Thomas W. Jacobs2
  • 1Michigan State University, United States
  • 2University of Illinois at Urbana-Champaign, United States
  • 3Donald Danforth Plant Science Center, United States

Stomata control water loss and carbon dioxide uptake by both altering pore aperture and developmental patterning. Stomatal patterning is regulated by environmental factors including atmospheric carbon dioxide (p[CO2]), which is increasing globally at an unprecedented rate. Mature leaves are known to convey developmental cues to immature leaves in response to p[CO2], but the developmental mechanisms are unknown. To characterize changes in stomatal patterning resulting from signals moving from mature to developing leaves, we constructed a dual-chamber growth system in which rosette and cauline leaves of Arabidopsis thaliana were subjected to differing p[CO2]. Young rosette tissue was found to adjust stomatal index (SI, the proportion of stomata to total cell number) in response to both the current environment and the environment experienced by mature rosette tissue, whereas cauline leaves appear to be insensitive to p[CO2] treatment. It is likely that cauline leaves and cotyledons deploy mechanisms for controlling stomatal development that share common but also deploy distinctive mechanisms to that operating in rosette leaves. The effect of p[CO2] on stomatal development is retained in cotyledons of the next generation, however this effect does not occur in pre-germination stomatal lineage cells but only after germination. Finally, these data suggest that p[CO2] affects regulation of stomatal development specifically through the development of satellite stomata (stomata induced by signals from a neighboring stomate) during spacing divisions and not the core pathway. To our knowledge, this is the first report identifying developmental steps responsible for altered stomatal patterning to p[CO2] and its trans-generational inheritance.

Keywords: Satellite stomata, Stomatal patterning, Long-distance signaling, dual-environment chambers, optical topometry, Persistent homology, Carbon Dioxide

Received: 20 Aug 2018; Accepted: 05 Nov 2018.

Edited by:

Stefan De Folter, Centro de Investigación y de Estudios Avanzados (CINVESTAV), Mexico

Reviewed by:

Yoshihisa Ueno, Ryukoku University, Japan
Caspar C. Chater, Faculty of Science, University of Sheffield, United Kingdom  

Copyright: © 2018 Haus, Li, Chitwood and Jacobs. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Miranda J. Haus, Michigan State University, East Lansing, United States, hausmira@msu.edu