Long-Distance and Trans-Generational Stomatal Patterning by CO2 Across Arabidopsis Organs

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.

A Genetic Dissection of Natural Variation for Stomatal Abundance Traits in Arabidopsis

“…It has been assumed that PL and SL contribute to the phenotypic plasticity of stomatal development in response to internal and environmental signals (Bergmann and Sack, 2007; Casson and Hetherington, 2010; Lampard, 2010). Supporting this view, recent work on the stomatal development responses (Haus et al, 2018) highlights the importance of SL in developmental plasticity in response to the atmospheric CO 2 concentration.…”

Effective range of non-cell autonomous activator and inhibitor peptides specifying plant stomatal patterning

“…Statistical methods of spatial point analysis from other fields have begun to be embraced, and it is vital to find the specific metric suitable for extracting the information each individual study needs. One such technique is the use of Betti numbers from persistent homology ( Haus et al, 2018 ). Applied to stomatal patterning, the 0th Betti number counts the number of stomata clusters (called ‘components’) across a leaf that remain separate when stomata are connected by a radius of given distance.…”

Heritable Changes in Physiological Gas Exchange Traits in Response to Long-Term, Moderate Free-Air Carbon Dioxide Enrichment

“…A review of plant responses to free-air [CO 2 ] enrichment indicates significant capacity for acclimation among modern plant taxa (Anderson et al, 2001; Drake et al, 1997; Maherali et al, 2002) and, in some cases, the capacity for those acclimations to be observable among offspring (Grossman and Rice, 2014; Haus et al, 2018; Li et al, 2019; Nakamura et al, 2011; Saban et al, 2019). However, there are a number of studies that specifically describe a lack of any acclamatory responses (Bader et al, 2010; Crous et al, 2011; Herrick and Thomas, 2001; Leakey et al, 2006; Usuda, 2006).…”

“…Whatever the mechanisms might be, highly dynamic stomatal control may confer an important WUE i advantage to taxa in terms of their resilience to the increasingly variable climatic conditions predicted in the near future (Hetherington and Woodward, 2003). It may be the case due to the observed differential capacities of individual species to increase WUE that some species will be better suited to future environments than others as increased WUEs will alter the ecological fitness of some taxa in comparison to neighboring competitors (Blumenthal et al, 2013; Grossman and Rice, 2014; Haus et al, 2018; Huxman and Smith, 2001).…”