Leaf trait covariation and controls on leaf mass per area (LMA) following cotton domestication

The process of domestication has driven dramatic shifts in plant
functional traits including leaf mass per area (LMA). It remains unclear
whether domestication has produced concerted shifts in the lower-level
anatomical traits that underpin LMA and how these traits in turn affect
photosynthesis. In this study, we investigated controls of LMA
and leaf gas exchange by leaf anatomical properties at the cellular,
tissue and whole leaf levels, comparing 26 wild and 31 domesticated
genotypes of cotton (Gossypium). As expected, domesticated plants
expressed lower LMA, higher photosynthesis and stomatal conductance,
suggesting a shift towards the ‘faster’ end of the leaf economics
spectrum. At whole-leaf level, variation in LMA was predominantly
determined by leaf density (LD) both in wild and domesticated genotypes.
At tissue level, higher leaf volume per area (Vleaf) in domesticated
genotypes was driven by a simultaneous increase in the volume of
epidermal, mesophyll and vascular bundle tissue and airspace, while lower
LD resulted from a dilution effect of lower increased volume of palisade
tissue and vascular bundle of high mass density by higher increased volume
of epidermis and airspace of low mass density. The volume of spongy
mesophyll exerted direct control on photosynthesis in domesticated
genotypes but only indirect control in wild genotypes. At cellular level,
a shift to larger but less numerous cells with thinner cell walls
underpinned a lower proportion of cell wall mass, and thus a reduction in
LD. Taken together, cotton domestication has triggered
synergistic shifts in the underlying determinants of LMA but also
photosynthesis, at cell, tissue and whole-leaf level, resulting in a
marked shift in plant ecological strategy.