Chloroplasts are best known for their role in photosynthesis, but they also allow nitrogen and sulphur assimilation, amino acid, fatty acid, nucleotide and hormone synthesis. How chloroplasts develop is therefore relevant to these diverse and fundamental biological processes, but also to attempts at their rational redesign. Light is strictly required for chloroplast formation in all angiosperms and directly regulates the expression of hundreds of chloroplast-related genes. Light also modulates the levels of several hormones including brassinosteriods, cytokinins, auxins and gibberellins, which themselves control chloroplast development particularly during early stages of plant development. Transcription factors such as GOLDENLIKE1&2 (GLK1&2), GATA NITRATE-INDUCIBLE CARBON METABOLISM-INVOLVED (GNC) and CYTOKININ-RESPONSIVE GATA FACTOR 1 (CGA1) act downstream of both light and phytohormone signalling to regulate chloroplast development. Thus, in green tissues transcription factors, light signalling and hormone signalling form a complex network regulating the transcription of chloroplast-and photosynthesis-related genes to control the development and number of chloroplasts per cell. We use this conceptual framework to identify points of regulation that could be harnessed to modulate chloroplast abundance and increase photosynthetic efficiency of crops, and to highlight future avenues to overcome gaps in current knowledge.

Soil salinization is increasing globally, driving a reduction in crop yields that threatens food security. Salinity stress reduces plant growth by exerting two stresses on plants: rapid shoot ion-independent effects which are largely osmotic and delayed ionic effects that are specific to salinity stress. In this study we set out to delineate the osmotic from the ionic effects of salinity stress. Arabidopsis thaliana plants were germinated and grown for two weeks in media supplemented with 50, 75, 100, or 125 mM NaCl (that imposes both an ionic and osmotic stress) or iso-osmolar concentrations (100, 150, 200, or 250 mM) of sorbitol, that imposes only an osmotic stress. A subsequent transcriptional analysis was performed to identify sets of genes that are differentially expressed in plants grown in (1) NaCl or (2) sorbitol compared to controls. A comparison of the gene sets identified genes that are differentially expressed under both challenge conditions (osmotic genes) and genes that are only differentially expressed in plants grown on NaCl (ionic genes, hereafter referred to as salt-specific genes). A pathway analysis of the osmotic and salt-specific gene lists revealed that distinct biological processes are modulated during growth under the two conditions. The list of salt-specific genes was enriched in the gene ontology (GO) term “response to auxin.” Quantification of the predominant auxin, indole-3-acetic acid (IAA) and IAA biosynthetic intermediates revealed that IAA levels are elevated in a salt-specific manner through increased IAA biosynthesis. Furthermore, the expression of NITRILASE 2 (NIT2), which hydrolyses indole-3-acetonitile (IAN) into IAA, increased in a salt-specific manner. Overexpression of NIT2 resulted in increased IAA levels, improved Na:K ratios and enhanced survival and growth of Arabidopsis under saline conditions. Overall, our data suggest that auxin is involved in maintaining growth during the ionic stress imposed by saline conditions.

Chilling stress has the potential to significantly decrease growth and yield of sensitive crop plants such as maize. Based on previous work, high light during chilling may exacerbate stress via enhanced photoinhibition but may also aid acclimation responses to chilling. To further understand molecular processes behind responses to chilling with and without high light, two maize accessions with contrasting tolerance (B73 and F7) were exposed to three treatments: chilling, chilling combined with high light and high light alone. Transcriptome data indicated that the chilling treatment resulted in the largest stress response. Addition of high light to chilling stress had a mitigating, rather than additive effect on stress, as evident from alleviated repression of photosynthesis-related genes and less induction of stress-related pathways such as abscisic acid signalling and senescence compared with the response to chilling alone. Five transcription factors belonging to well-known stress-related transcription factor families were identified as candidates for driving the transcriptional changes behind the high-light induced mitigation of chilling stress. Physiological measurements of non-photochemical quenching and the maximum quantum efficiency of photosystem II corroborated the transcriptome results, showing that the addition of high light alleviated photoinhibition and membrane damage caused by chilling. High light alone had little effect on the plant transcriptome or physiological response. Overall, this study overturns previous reports, offers a new outlook on the impact of high light during chilling stress and has the potential to provide clearer targets for crop engineering.