Phenotypic and Genetic Variation in Morphophysiological Traits in Huanglongbing-Affected Mandarin Hybrid Populations

Huanglongbing (HLB) caused by 'Candidatus Liberibacter asiaticus' (CLas) is the most costly disease for the global citrus industry. Currently, no effective tools have been found to control HLB. Most commercial citrus varieties are susceptible to HLB, though some citrus hybrid cultivars have reduced sensitivity to the disease. Citrus breeding populations contain a large diversity of germplasm, with thousands of unique genotypes exhibiting a broad range of phenotypes. Understanding phenotypic variation and genetic inheritance in HLB-affected mandarin hybrid populations are crucial for breeding tolerant citrus varieties. In this study, we assessed 448 diverse mandarin hybrids coming from 30 crosses, and 45 additional accessions. For HLB tolerance, we measured HLB severity visual score and CLas titers by qPCR. We also measured seven morphophysiological traits indirectly related to HLB tolerance with leaf area index (LAI), leaf area (LA), leaf mass per area (LMA), photosystem II parameters (Fv/Fo, Fv/Fm), and photochemical performance index (PI_abs). By estimating the genetic variation in five half-sib families, we estimated the heritability of phenotypic traits and found a significant genetic effect on HLB visual score and photosynthesis parameters, which indicates opportunities for the genetic improvement of HLB tolerance. In addition, although it is easy to identify infected trees based on HLB symptomatic leaves, visually phenotyping whole trees can be difficult and inconsistent due to the interpersonal subjectivity of characterization. We investigated their relationships and found that LAI was highly correlated with HLB score, with correlation coefficients of r = 0.70 and r = 0.77 for the whole population and five half-sib families, respectively. Photochemical parameters showed significant correlation with HLB severity and responded differentially with the side of the canopy. Our study suggests that LAI and photochemical parameters could be used as a rapid and cost-effective method to evaluate HLB tolerance and inheritance in citrus breeding programs.