Whole organ, venation and epidermal cell morphological variations are correlated in the leaves of Arabidopsis mutants

Abstract

Despite the large number of genes known to affect leaf shape or size, we still have a relatively poor understanding of how leaf morphology is established. For example, little is known about how cell division and cell expansion are controlled and coordinated within a growing leaf to eventually develop into a laminar organ of a definite size. To obtain a global perspective of the cellular basis of variations in leaf morphology at the organ, tissue and cell levels, we studied a collection of 111 non-allelic mutants with abnormally shaped and/or sized leaves, which broadly represent the mutational variations in Arabidopsis thaliana leaf morphology not associated with lethality. We used image-processing techniques on these mutants to quantify morphological parameters running the gamut from the palisade mesophyll and epidermal cells to the venation, whole leaf and rosette levels. We found positive correlations between epidermal cell size and leaf area, which is consistent with long-standing Avery's hypothesis that the epidermis drives leaf growth. In addition, venation parameters were positively correlated with leaf area, suggesting that leaf growth and vein patterning share some genetic controls. Positional cloning of the genes affected by the studied mutations will eventually establish functional links between genotypes, molecular functions, cellular parameters and leaf phenotypes. A morphometric analysis of more than one hundred Arabidopsis leaf mutants suggests the nonessential contribution of the inner tissue layers to leaf morphogenesis and supports the idea that the epidermis drives leaf growth. Also, we provide the scientific community with some cellular descriptors that will allow the reinterpretation of already published leaf mutant phenotypes. © 2011 Blackwell Publishing Ltd.