Abstract
Through microscopic analysis of veins and assessment of light- and CO2-saturated rates of photosynthetic oxygen evolution, we investigated the relationship between minor loading vein anatomy and photosynthesis of mature leaves in three ecotypes of Arabidopsis thaliana grown under four different combinations of temperature and photon flux density (PFD). All three ecotypes exhibited greater numbers and cross-sectional area of phloem cells as well as higher photosynthesis rates in response to higher PFD and especially lower temperature. The Swedish ecotype exhibited the strongest response to these conditions, the Italian ecotype the weakest response, and the Col-0 ecotype exhibited an intermediate response. Among all three ecotypes, strong linear relationships were found between light- and CO2-saturated rates of photosynthetic oxygen evolution and the number and area of either sieve elements or of companion and phloem parenchyma cells in foliar minor loading veins, with the Swedish ecotype showing the highest number of cells in minor loading veins (and largest minor veins) coupled with unprecedented high rates of photosynthesis. Linear, albeit less significant, relationships were also observed between number and cross-sectional area of tracheids per minor loading vein versus light- and CO2-saturated rates of photosynthetic oxygen evolution. We suggest that sugar distribution infrastructure in the phloem is co-regulated with other features that set the upper limit for photosynthesis. The apparent genetic differences among Arabidopsis ecotypes should allow for future identification of the gene(s) involved in augmenting sugar-loading and -transporting phloem cells and maximal rates of photosynthesis.
Highlights
Attempts to increase photosynthetic rate through overexpression of key components of the photosynthetic process have met with surprisingly little success (Micallef et al, 1995; Miyagawa et al, 2001; Lefebvre et al, 2005; Feng et al, 2007a,b; Kebeish et al, 2007; Rosenthal et al, 2011)
An extensive and comprehensive characterization of many different aspects of phloem anatomy was initially conducted. Those characteristics of the phloem that exhibited the greatest co-variation in response to the environment were explored here with respect to their relationship with photosynthesis
Growth under higher photon flux density (PFD) and lower temperature resulted in greater rates of light- and CO2-saturated photosynthetic oxygen evolution (Figure 1A) as well as greater cross-sectional areas of the phloem portion (Figure 1B) of foliar minor loading veins in the Italian, Col-0, and Swedish ecotypes
Summary
Attempts to increase photosynthetic rate through overexpression of key components of the photosynthetic process have met with surprisingly little success (Micallef et al, 1995; Miyagawa et al, 2001; Lefebvre et al, 2005; Feng et al, 2007a,b; Kebeish et al, 2007; Rosenthal et al, 2011). Any limitations were to exist to the export of products of photosynthesis from the leaf to the rest of the plant, one should, not expect increases in photosynthesis rate from overexpression of photosynthetic genes. In such an event, the well-known feedback inhibition by accumulated products of photosynthesis, via repression of photosynthetic genes (Krapp and Stitt, 1995; Paul and Foyer, 2001) and, possibly, sucrose transporter genes in apoplastic loaders (Vaughn et al, 2002), would be expected to counteract or abolish effects of overexpression of photosynthetic genes. These measurements of the leaf ’s CO2 fixation rates reflect barriers to CO2 movement from the atmosphere to the carboxylation sites in the chloroplasts (cuticular, stomatal, mesophyll, cell wall, and chloroplast envelope resistances; Boyer et al, 1997; Tuzet et al, 2003; Tholen and Zhu, 2011; Flexas et al, 2012), and do not measure the leaf ’s intrinsic maximal capacity www.frontiersin.org
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