Abstract
An Arabidopsis thaliana accession with naturally low vein density, Eifel-5 (Ei-5), was compared to Columbia-0 (Col-0) with respect to rosette growth, foliar vein architecture, photosynthesis, and transpiration. In addition to having to a lower vein density, Ei-5 grew more slowly, with significantly lower rates of rosette expansion, but had similar capacities for photosynthetic oxygen evolution on a leaf area basis compared to Col-0. The individual foliar minor veins were larger in Ei-5, with a greater number of vascular cells per vein, compared to Col-0. This compensation for low vein density resulted in similar values for the product of vein density × phloem cell number per minor vein in Ei-5 and Col-0, which suggests a similar capacity for foliar sugar export to support similar photosynthetic capacities per unit leaf area. In contrast, the product of vein density × xylem cell number per minor vein was significantly greater in Ei-5 compared to Col-0, and was associated not only with a higher ratio of water-transporting tracheary elements versus sugar-transporting sieve elements but also significantly higher foliar transpiration rates per leaf area in Ei-5. In contrast, previous studies in other systems had reported higher ratios of tracheary to sieve elements and higher transpiration rate to be associated with higher – rather than lower – vein densities. The Ei-5 accession thus further underscores the plasticity of the foliar vasculature by illustrating an example where a higher ratio of tracheary to sieve elements is associated with a lower vein density. Establishment of the Ei-5 accession, with a low vein density but an apparent overcapacity for water flux through the foliar xylem network, may have been facilitated by a higher level of precipitation in its habitat of origin compared to that of the Col-0 accession.
Highlights
IntroductionThe maximal capacity of a leaf to carry out photosynthesis is closely coordinated with the capacity of the foliar vasculature for sugar and water transport, and these features co-vary in response to the growth environment as has been documented in several genotypes of the winter annual Arabidopsis thaliana (Cohu et al, 2013a,b; Adams et al, 2016; Stewart et al, 2016, 2017a,b, 2018)
Minor-vein density was significantly lower in Ei-5 compared to Col-0 (Figure 5A and Table 1), but the number of vascular cells per minor vein was significantly greater in Ei-5 (Figure 5B and Table 1)
These latter two differences compensated for each other, and total vascular cell number normalized for vein density was the same in the two accessions, as ascertained by multiplication of foliar vein density × the number of vascular cells per minor vein (Figure 5C and Table 1)
Summary
The maximal capacity of a leaf to carry out photosynthesis is closely coordinated with the capacity of the foliar vasculature for sugar and water transport, and these features co-vary in response to the growth environment as has been documented in several genotypes of the winter annual Arabidopsis thaliana (Cohu et al, 2013a,b; Adams et al, 2016; Stewart et al, 2016, 2017a,b, 2018). Vein Anatomy Compensates for Density (Amiard et al, 2005; Adams et al, 2007, 2013a, 2016; Dumlao et al, 2012; Muller et al, 2014b; Stewart et al, 2016, 2017a,b), number of vascular cells per minor vein (Adams et al, 2013a, 2016; Cohu et al, 2013a,b, 2014; Muller et al, 2014b; Stewart et al, 2016, 2017a,b), size of individual vascular cells (Adams et al, 2013a; Muller et al, 2014b; Stewart et al, 2017a,b), and the ultrastructure of phloem transfer cells (Amiard et al, 2005, 2007; Adams et al, 2014a, 2016) Such modulation of foliar vascular features is predicted to support photosynthesis as the need for water import and sugar export change in response to the growth environment. Acclimation to high versus low light involved parallel upregulation of foliar vascular features associated with higher capacities for both sugar and water transport, of photosynthetic capacities, and of transpiration rates (Stewart et al, 2017a,b)
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