Abstract
Leaves comprise multiple cell types but our knowledge of the patterns of
gene expression that underpin their functional specialization is fragmentary.
Our understanding and ability to undertake rational redesign of these cells is
therefore limited. We aimed to identify genes associated with the incompletely
understood bundle sheath of C3 plants, which represents a
key target associated with engineering traits such as C4
photosynthesis into rice. To better understand veins, bundle sheath and
mesophyll cells of rice we used laser capture microdissection followed by deep
sequencing. Gene expression of the mesophyll is conditioned to allow coenzyme
metabolism and redox homeostasis as well as photosynthesis. In contrast, the
bundle sheath is specialized in water transport, sulphur assimilation and
jasmonic acid biosynthesis. Despite the small chloroplast compartment of bundle
sheath cells, substantial photosynthesis gene expression was detected. These
patterns of gene expression were not associated with presence/absence of
particular transcription factors in each cell type, but rather gradients in
expression across the leaf. Comparative analysis with
C3Arabidopsis identified a
small gene-set preferentially expressed in bundle sheath cells of both species.
This included genes encoding transcription factors from fourteen orthogroups,
and proteins allowing water transport, sulphate assimilation and jasmonic acid
synthesis. The most parsimonious explanation for our findings is that bundle
sheath cells from the last common ancestor of rice and Arabidopsis was
specialized in this manner, and since the species diverged these patterns of
gene expression have been maintained.
Significance statement
The role of bundle sheath cells in C4 species have
been studied intensively but this is not the case in leaves that use the
ancestral C3 pathway. Here, we show that gene
expression in the bundle sheath of rice is specialized to allow sulphate and
nitrate reduction, water transport and jasmonate synthesis, and comparative
analysis with Arabidopsis indicates ancient roles for bundle sheath cells in
water transport, sulphur and jasmonate synthesis.
The contributions of apoplastic, symplastic and gas phase pathways for water transport outside the bundle sheath in leaves