Disruption of <i>CYCLOPHILIN 38</i> Function Reveals a Photosynthesis-Dependent Systemic Signal Controlling Lateral Root Emergence

Abstract

Photosynthesis in leaves generates the fixed-carbon resources and essential metabolites that support sink tissues, such as roots. One of these products, sucrose, is known to promote primary root growth, but it is not clear what other molecules may be involved and whether other stages of root system development are affected by photosynthate levels. Through a mutant screen to identify pathways regulating root system architecture, we identified a mutation in the CYCLOPHILIN 38 (CYP38) gene, which causes an accumulation of pre-emergent stage lateral roots, with a minor effect on primary root growth. CYP38 was previously reported to maintain the stability of Photosystem II (PSII) in chloroplasts. CYP38 expression is enriched in the shoot and grafting experiments show that the gene acts non-cell autonomously to promote lateral root emergence. Growth of wild-type plants under low light conditions phenocopied the cyp38 lateral root emergence phenotype as did the inhibition of PSII-dependent electron transport or NADPH production. Importantly, the cyp38 root phenotype is not rescued by exogenous sucrose, suggesting the involvement of another metabolite. Auxin (IAA) is an essential hormone promoting root growth and its biosynthesis from tryptophan is dependent on reductant generated during photosynthesis. Both WT seedlings grown under low light and cyp38 mutants have highly diminished levels of IAA in root tissues. The cyp38 lateral root defect is rescued by IAA treatment, revealing that photosynthesis promotes lateral root emergence partly through IAA biosynthesis. Metabolomic profiling shows that the accumulation of several defense-related metabolites are also photosynthesis-dependent, suggesting that the regulation of a number of energy-intensive pathways are down-regulated when light becomes limiting.