Abstract
C(4) photosynthesis has evolved in at least 66 lineages within the angiosperms and involves alterations to the biochemistry, cell biology, and development of leaves. The characteristic "Kranz" anatomy of most C(4) leaves was discovered in the 1890s, but the genetic basis of these traits remains poorly defined. Oat × maize addition lines allow the effects of individual maize (Zea mays; C(4)) chromosomes to be investigated in an oat (Avena sativa; C(3)) genetic background. Here, we have determined the extent to which maize chromosomes can introduce C(4) characteristics into oat and have associated any C(4)-like changes with specific maize chromosomes. While there is no indication of a simultaneous change to C(4) biochemistry, leaf anatomy, and ultrastructure in any of the oat × maize addition lines, the C(3) oat leaf can be modified at multiple levels. Maize genes encoding phosphoenolpyruvate carboxylase, pyruvate, orthophosphate dikinase, and the 2'-oxoglutarate/malate transporter are expressed in oat and generate transcripts of the correct size. Three maize chromosomes independently cause increases in vein density, and maize chromosome 3 results in larger bundle sheath cells with increased cell wall lipid deposition in oat leaves. These data provide proof of principle that aspects of C(4) biology could be integrated into leaves of C(3) crops.
Highlights
Causes Lipid Deposition in Oat PBS Cell WallsIn order to determine the extent to which the enlarged PBS cells in oat maize addition lines (OMAs) 3.01 resembled the maize PBS, transverse sections of leaves were stained with Nile red to detect fatty acid deposition
In order to investigate whether the presence of individual maize chromosomes increased venation in oat, distances between the midpoints of adjacent veins were measured in transverse sections of fully expanded third leaves from OMA lines via light microscopy
Intervein distance (IVD) in OMA lines was variable, indicating that individual maize chromosomes in the oat background exerted an influence on vein spacing (Fig. 1A)
Summary
Causes Lipid Deposition in Oat PBS Cell WallsIn order to determine the extent to which the enlarged PBS cells in OMA 3.01 resembled the maize PBS, transverse sections of leaves were stained with Nile red to detect fatty acid deposition. Nile red stains positively for lipids in plants (Fowler and Greenspan, 1985; Greenspan and Fowler, 1985; Greenspan et al, 1985; Pighin et al, 2004; Schmidt and Herman, 2008; Dietrich et al, 2009), fluorescing red in the presence of polar lipids and yellow when staining esterified cholesterol and triacylglycerols (Diaz et al, 2008) This approach showed polar lipids in the PBS of maize, but in the oat parental line, only the MS and some of the veinal cells stained (Fig. 2, A and B). Transmission electron microscopy (TEM) imaging of the leaves indicated the presence of suberin in the cell walls of the PBS in maize but only in the MS cell layer of OMA 3.01 and wildtype oat (Fig. 2, D–F). These data indicate that chromosome 3 likely contains loci that can control PBS cell wall lipid deposition in oat but not the entire suberin deposition pathway
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