The bundle sheath of rice is conditioned to play an active role in water transport as well as sulfur assimilation and jasmonic acid synthesis

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 the rational redesign of these cells is therefore limited. We aimed to identify genes associated with the incompletely understood bundle sheath of C 3 plants, which represents a key target associated with engineering traits such as C 4 photosynthesis into Oryza sativa (rice). To better understand the 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 the presence or absence of specific transcription factors in each cell type, but were instead associated with gradients in expression across the leaf. Comparative analysis with C 3 Arabidopsis identified a small gene set preferentially expressed in the bundle sheath cells of both species. This gene set included genes encoding transcription factors from 14 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 were specialized in this manner, and as the species diverged these patterns of gene expression have been maintained.

Distinct C4 sub‐types and C3 bundle sheath isolation in the Paniceae grasses

“…We do note, however, that some sulfur metabolism‐related genes shown to be enriched in Arabidopsis BS were actually found to be depleted in the S. indica BS. Overall, the S. indica BS samples are highly consistent with previous studies on Arabidopsis and rice BS, indicating both the validity of the mechanical C 3 BS isolation done here and the conservation of C 3 functions across these divergent species (Aubry et al, 2014 ; Hua et al, 2021 ).…”

Chloroplast development in green plant tissues: the interplay between light, hormone, and transcriptional regulation

“…Transcription factors such as GOLDEN2‐LIKE 1 and 2 ( GLK1&2 ), GATA NITRATE‐INDUCIBLE CARBON‐METABOLISM‐INVOLVED ( GNC ) and CYTOKININ‐RESPONSIVE GATA FACTOR 1 ( CGA1 ) are involved in chloroplast biogenesis during all stages of plant growth. Their expression levels differ between cell types and during leaf development, likely contributing to observed differences in chloroplast development (Waters et al ., 2008; Wang et al ., 2017a; Hua et al ., 2021). As these transcription factors have homologues in all plants studied to date and act as key integrators of light and hormone signalling (Figs 2, 8) they are considered the closest that we know of to master regulators of chloroplast development.…”

Sulfur Stable Isotope Discrimination in Rice: A Sulfur Isotope Mass Balance Study

“…Such a discrepancy might depend on the growth conditions (closed hydroponic-plant system vs. field) or, more likely, on the different S nutritional status and/or growth stage of the plants considered in the two studies since S stable isotope separations conserve the memory of the physiological and metabolic activities that determined them. Finally, differences may also originate from the different distribution of the S assimilation enzymes in the leaf, since rice assimilates SO 4 2− mainly in the bundle sheaths, while other species, also in the mesophyll (Hua et al, 2021). The isotope composition of the SO 4 2− pools of the root was lighter relative to the S source but heavier with respect to the expected composition calculated according to the isotope discrimination occurring during SO 4 2− uptake at high external concentrations [i.e., δ 34 S_SO 4 2− > δ 34 S_SO 4 2− source -1(L/H ) ].…”

“…Such a discrepancy might depend on the growth conditions (closed hydroponic-plant system vs. field) or, more likely, on the different S nutritional status and/or growth stage of the plants considered in the two studies since S stable isotope separations conserve the memory of the physiological and metabolic activities that determined them. Finally, differences may also originate from the different distribution of the S assimilation enzymes in the leaf, since rice assimilates SO 4 2– mainly in the bundle sheaths, while other species, also in the mesophyll ( Hua et al, 2021 ).…”