Common-Garden Transcriptomes Distinguish Leaf-Form-Associated from Site-Associated Expression in Zygophyllum xanthoxylum

Zygophyllum xanthoxylum (Bunge) Maxim. is a dominant, deep-rooted shrub of the temperate deserts of north-western China whose leaflets range from comparatively flat and broad to slender and terete, but the molecular basis of this variation has rarely been reported. We compared three accessions from contrasting desert habitats—one flat-leaved, from a shaded high-altitude valley, and two rod-leaved, from open full-sun sites. The accessions differed in the leaflet blade but not in the petiole, the flat-leaved accession bearing shorter and much wider leaflets with a width-to-length ratio almost four times greater. Leaf transcriptomes were assembled, and pairwise comparison identified several thousand differentially expressed genes. The leaf-form signal was defined as the genes that changed concordantly in both flat-versus-rod comparisons, placing the flat-leaved accession at one extreme of the series. This set contains a reciprocal leaf-development module: the YABBY lamina gene YAB2, the auxin/polarity factors ARF3 and ARF18 and the expansin EXPA1 are higher in the flat-leaved accession, whereas the KNOX gene KNAT6, the class II TCP gene TCP12, ARF6, EXPA4 and ATHB7 are higher in both rod-leaved accessions. Photosynthesis genes are significantly concentrated in the expression clusters that peak in the flat-leaved accession, with light-harvesting antenna, photosystem II and Calvin-cycle transcripts highest there. The chlorophyll a-b binding protein CAB and the cytosolic phosphoglycerate kinase PGK are the most strongly flat-biased transcripts, and in each case, the bias holds for the gene family as a whole; quantitative RT-PCR confirmed the sequencing-based estimates. Flat- versus rod-leaved differentiation in Z. xanthoxylum is therefore accompanied by constitutive, coordinated differences in leaf-development and light-harvesting gene expression, CAB and PGK are proposed as candidate expression markers of the flat-leaved form.