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

Abstract

Stomatal abundance varies widely across natural populations of Arabidopsis thaliana, and presumably affects plant performance because it influences water and CO2 exchange with the atmosphere and thence photosynthesis and transpiration. In order to determine the genetic basis of this natural variation, we have analyzed a recombinant inbred line (RIL) population derived from the wild accession Ll-0 and the reference strain Landsberg erecta (Ler), which show low and high stomatal abundance, respectively. Quantitative trait locus (QTL) analyses of stomatal index, stomatal density, and pavement cell density measured in the adaxial cotyledon epidermis, identified five loci. Three of the genomic regions affect all traits and were named MID (Modulator of Cell Index and Density) 1 to 3. MID2 is a large-effect QTL overlapping with ERECTA (ER), the er-1 allele from Ler increasing all trait values. Additional analyses of natural and induced loss-of-function er mutations in different genetic backgrounds revealed that ER dysfunctions have differential and opposite effects on the stomatal index in adaxial and abaxial cotyledon epidermis and confirmed that ER is the gene underlying MID2. Ll-0 alleles at MID1 and MID3 displayed moderate and positive effects on the various traits. Furthermore, detailed developmental studies tracking primary and satellite stomatal lineages show that MID3-Ll-0 allele promotes the spacing divisions that initiate satellite lineages, while the ER allele limits them. Finally, expression analyses suggest that ER and MID3 modulate satellization through partly different regulatory pathways. Our characterization of MID3 indicates that genetic modulation of satellization contributes to the variation for stomatal abundance in natural populations, and subsequently that this trait might be involved in plant adaptation.

Optical topometry and machine learning to rapidly phenotype stomatal patterning traits for maize QTL mapping

“…The number and strength of QTL identified for leaf gas exchange traits (1–4 QTL per trait in a single experiment) were similar to previous studies of those traits ( Hervé et al, 2001 ; Teng et al, 2004 ; Pelleschi et al, 2006 ). In contrast, a greater number of QTL were identified for many of the stomatal patterning traits (e.g., PD—7, SI—9, SCA—9, SCD—9, SCTA—7 QTL in a single experiment) than in previous studies ( Patto et al, 2003 ; Hall et al, 2005 ; Laza et al, 2010 ; Schoppach et al, 2016 ; Shahinnia et al, 2016 ; Liu et al, 2017 ; Sumathi et al, 2018 ; Delgado et al, 2019 ; Prakash et al, 2020 ). This larger number of significant QTL was linked to more small-effect QTL (PVE < 10%) being successfully identified.…”

Stomatal patterning is differently regulated in adaxial and abaxial epidermis in Arabidopsis

“…Stomatal ratio did not differ between leaves in any of our studied genotypes (Figure 1D). However, the stomatal ratio values that we measured in true leaves of wild-type plants were higher than reported before in cotyledons (Geisler et al ., 1998; Berger and Altmann, 2000; Delgado et al ., 2019), indicating that there is within-plant variation also in leaf stomatal ratio. Differences between stomatal characteristics depending on leaf number have been discussed before, stressing more severe effects of different mutations on stomatal development in cotyledons than in true leaves (Dow et al ., 2014).…”

The Genetic Control of Stomatal Development in Barley: New Solutions for Enhanced Water-Use Efficiency in Drought-Prone Environments

“…There exists a generous level of data underlying the genetic basis of drought tolerance. However, a substantial investigation is yet to be conducted regarding the molecular characterisation of barley stomatal development, despite stomatal density and morphology being repeatedly documented as major contenders for the genetic improvement of WUE, in addition to possessing relatively high values of heritability [62,131,132]. This situation is made further urgent by the fact that no data currently exists on the identification of critical genes in barley stomatal development.…”