Abstract
The husk surrounding the ear of corn/maize (Zea mays) has widely spaced veins with a number of interveinal mesophyll (M) cells and has been described as operating a partial C(3) photosynthetic pathway, in contrast to its leaves, which use the C(4) photosynthetic pathway. Here, we characterized photosynthesis in maize husk and leaf by measuring combined gas exchange and carbon isotope discrimination, the oxygen dependence of the CO(2) compensation point, and photosynthetic enzyme activity and localization together with anatomy. The CO(2) assimilation rate in the husk was less than that in the leaves and did not saturate at high CO(2), indicating CO(2) diffusion limitations. However, maximal photosynthetic rates were similar between the leaf and husk when expressed on a chlorophyll basis. The CO(2) compensation points of the husk were high compared with the leaf but did not vary with oxygen concentration. This and the low carbon isotope discrimination measured concurrently with gas exchange in the husk and leaf suggested C(4)-like photosynthesis in the husk. However, both Rubisco activity and the ratio of phosphoenolpyruvate carboxylase to Rubisco activity were reduced in the husk. Immunolocalization studies showed that phosphoenolpyruvate carboxylase is specifically localized in the layer of M cells surrounding the bundle sheath cells, while Rubisco and glycine decarboxylase were enriched in bundle sheath cells but also present in M cells. We conclude that maize husk operates C(4) photosynthesis dispersed around the widely spaced veins (analogous to leaves) in a diffusion-limited manner due to low M surface area exposed to intercellular air space, with the functional role of Rubisco and glycine decarboxylase in distant M yet to be explained.
Highlights
The husk surrounding the ear of corn/maize (Zea mays) has widely spaced veins with a number of interveinal mesophyll (M) cells and has been described as operating a partial C3 photosynthetic pathway, in contrast to its leaves, which use the C4 photosynthetic pathway
The partitioning of these two cycles is facilitated by two specialized photosynthetic cell types within the leaf: the bundle sheath (BS) cells, which are clustered around vascular bundles (VB) and are surrounded by mesophyll (M) cells, forming a wreath-like formation known as Kranz anatomy (Dengler and Nelson, 1999)
Our observations and measurements have shown that in maize, the outer husk surrounding the ear operates a C4-like photosynthetic pathway. Both carbon isotope analysis and the lack of oxygen sensitivity in the compensation point show that the majority of Rubisco actively participating in CO2 assimilation is that compartmentalized within the chloroplasts of BS cells, which is supported by the C4 cycle via phosphoenolpyruvate carboxylase (PEPC) in the adjacent M
Summary
The husk surrounding the ear of corn/maize (Zea mays) has widely spaced veins with a number of interveinal mesophyll (M) cells and has been described as operating a partial C3 photosynthetic pathway, in contrast to its leaves, which use the C4 photosynthetic pathway. The CO2 compensation points of the husk were high compared with the leaf but did not vary with oxygen concentration This and the low carbon isotope discrimination measured concurrently with gas exchange in the husk and leaf suggested C4-like photosynthesis in the husk. The maize (Zea mays) leaf utilizes CO2 to make sugars using the C4 photosynthetic pathway, in which carbon assimilation is essentially split into two distinct cycles within the leaf The partitioning of these two cycles is facilitated by two specialized photosynthetic cell types within the leaf: the bundle sheath (BS) cells, which are clustered around vascular bundles (VB) and are surrounded by mesophyll (M) cells, forming a wreath-like formation known as Kranz anatomy (Dengler and Nelson, 1999). Further evidence for this theory was reported by Yakir et al (1991), who measured the natural abundance of carbon isotopes (13C and 12C) in maize husk and leaf dry matter, calculating that there was significant C3 fixation of CO2 in the husk, contributing to the production of husk cellulose (16%)
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