Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development.

Understanding how plants grow is critical for agriculture and fundamental for illuminating principles of multicellular development. Here, we apply desorption electrospray ionization mass spectrometry imaging (DESI-MSI) to the chemical mapping of the developing maize root. This technique reveals a range of small molecule distribution patterns across the gradient of stem cell differentiation in the root. To understand the developmental logic of these patterns, we examine tricarboxylic acid (TCA) cycle metabolites. In both Arabidopsis and maize, we find evidence that elements of the TCA cycle are enriched in developmentally opposing regions. We find that these metabolites, particularly succinate, aconitate, citrate, and α-ketoglutarate, control root development in diverse and distinct ways. Critically, the developmental effects of certain TCA metabolites on stem cell behavior do not correlate with changes in ATP production. These results present insights into development and suggest practical means for controlling plant growth.

Non-canonical and developmental roles of the TCA cycle in plants.

Over recent years, our understanding of the tricarboxylic acid cycle (TCAC) in living organisms has expanded beyond its canonical role in cellular energy production. In plants, TCAC metabolites and related enzymes have important roles in physiology, including vacuolar function, chelation of metals and nutrients, photorespiration, and redox regulation. Research in other organisms, including animals, has demonstrated unexpected functions of the TCAC metabolites in a number of biological processes, including signaling, epigenetic regulation, and cell differentiation. Here, we review the recent progress in discovery of non-canonical roles of the TCAC. We then discuss research on these metabolites in the context of plant development, with a focus on research related to tissue-specific functions of the TCAC. Additionally, we review research describing connections between TCAC metabolites and phytohormone signaling pathways. Overall, we discuss the opportunities and challenges in discovering new functions of TCAC metabolites in plants.