Regulatory gateways for cell-specific gene expression in C4 leaves with Kranz anatomy.

C4 photosynthesis is a carbon-concentrating mechanism that increases delivery of carbon dioxide to RuBisCO and as a consequence reduces photorespiration. The C4 pathway is therefore beneficial in environments that promote high photorespiration. This pathway has evolved many times, and involves restricting gene expression to either mesophyll or bundle sheath cells. Here we review the regulatory mechanisms that control cell-preferential expression of genes in the C4 cycle. From this analysis, it is clear that the C4 pathway has a complex regulatory framework, with control operating at epigenetic, transcriptional, post-transcriptional, translational, and post-translational levels. Some genes of the C4 pathway are regulated at multiple levels, and we propose that this ensures robust expression in each cell type. Accumulating evidence suggests that multiple genes of the C4 pathway may share the same regulatory mechanism. The control systems for C4 photosynthesis gene expression appear to operate in C3 plants, and so it appears that pre-existing mechanisms form the basis of C4 photosynthesis gene expression.

Next-generation ABACUS biosensors reveal cellular ABA dynamics driving root growth at low aerial humidity.

The plant hormone abscisic acid (ABA) accumulates under abiotic stress to recast water relations and development. To overcome a lack of high-resolution sensitive reporters, we developed ABACUS2s-next-generation Förster resonance energy transfer (FRET) biosensors for ABA with high affinity, signal-to-noise ratio and orthogonality-that reveal endogenous ABA patterns in Arabidopsis thaliana. We mapped stress-induced ABA dynamics in high resolution to reveal the cellular basis for local and systemic ABA functions. At reduced foliar humidity, root cells accumulated ABA in the elongation zone, the site of phloem-transported ABA unloading. Phloem ABA and root ABA signalling were both essential to maintain root growth at low humidity. ABA coordinates a root response to foliar stresses, enabling plants to maintain foraging of deeper soil for water uptake.

Ancestral light and chloroplast regulation form the foundations for C4 gene expression.

C4 photosynthesis acts as a carbon concentrating mechanism that leads to large increases in photosynthetic efficiency. The C4 pathway is found in more than 60 plant lineages1 but the molecular enablers of this evolution are poorly understood. In particular, it is unclear how non-photosynthetic proteins in the ancestral C3 system have repeatedly become strongly expressed and integrated into photosynthesis gene regulatory networks in C4 leaves. Here, we provide clear evidence that in C3 leaves, genes encoding key enzymes of the C4 pathway are already co-regulated with photosynthesis genes and are controlled by both light and chloroplast-to-nucleus signalling. In C4 leaves this regulation becomes increasingly dependent on the chloroplast. We propose that regulation of C4 cycle genes by light and the chloroplast in the ancestral C3 state has facilitated the repeated evolution of the complex and convergent C4 trait.