Abstract

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 basal 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.

Highlights

  • Stomata are microscopic pores on the plant epidermis whose controlled opening and closing regulates carbon dioxide uptake and transpirational water loss

  • Previous studies had suggested that mature rosette leaves of Arabidopsis perceive environmental conditions and transduce those perceptions into a mobile signal that influences stomatal density and index in subsequently emerging leaves (Lake et al, 2001; Coupe et al, 2006)

  • We set out to test the hypothesis that a mobile signal from mature leaves directs stomatal development in emerging leaves based on the p[CO2] of the formers’ environment

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Summary

Introduction

Stomata are microscopic pores on the plant epidermis whose controlled opening and closing regulates carbon dioxide uptake and transpirational water loss. Long-Distance Stomatal Patterning by CO2 density and distribution of stomata over each leaf ’s surface. Both stomatal density (SD, number of stomata per mm2) and stomatal index (SI, proportion of stomata per total epidermal cell number) are responsive to the plant’s perception of humidity, light quality and quantity, and p[CO2] (Woodward and Kelly, 1995; Lake and Woodward, 2008; Casson et al, 2009; Kang et al, 2009; Pillitteri and Torii, 2012; Šantrucek et al, 2014). When we consider the environmental effect of doubling p[CO2], SI usually decreases by an average 29%, but large variation exists both within and across species such that increased SI is not uncommon (Woodward and Kelly, 1995; Woodward et al, 2002). The inverse correlation between SI and p[CO2] within indicator species is sufficiently strong that SI in fossilized or dried leaves is a proxy for paleoclimates’ p[CO2] (McElwain et al, 1999; Beerling and Royer, 2002; Steinthorsdottir et al, 2011)

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