Genome-wide association study of cyanogenic glycosides, proline, sugars, and pigments in Eucalyptus cladocalyx after 18 consecutive dry summers

Natural variation of cyanogenic glycosides, soluble sugars, proline, and nondestructive optical sensing of pigments (chlorophyll, flavonols, and anthocyanins) was examined in ex situ natural populations of Eucalyptus cladocalyx F. Muell. grown under dry environmental conditions in the southern Atacama Desert, Chile. After 18 consecutive dry seasons, considerable plant-to-plant phenotypic variation for all the traits was observed in the field. For example, leaf hydrogen cyanide (HCN) concentrations varied from 0 (two acyanogenic individuals) to 1.54 mg cyanide g⁻¹ DW. Subsequent genome-wide association study revealed associations with several genes with a known function in plants. HCN content was associated robustly with genes encoding Cytochrome P450 proteins, and with genes involved in the detoxification mechanism of HCN in cells (β-cyanoalanine synthase and cyanoalanine nitrilase). Another important finding was that sugars, proline, and pigment content were linked to genes involved in transport, biosynthesis, and/or catabolism. Estimates of genomic heritability (based on haplotypes) ranged between 0.46 and 0.84 (HCN and proline content, respectively). Proline and soluble sugars had the highest predictive ability of genomic prediction models (PA = 0.65 and PA = 0.71, respectively). PA values for HCN content and flavonols were relatively moderate, with estimates ranging from 0.44 to 0.50. These findings provide new understanding on the genetic architecture of cyanogenic capacity, and other key complex traits in cyanogenic E. cladocalyx.