Sink formation during shoot infection of tomato Micro-Tom by Moniliophthora perniciosa , the causal agent of cacao witches' broom disease, limits sugar supply for effective development of lateral roots

Moniliophthora perniciosa causes the witches’ broom disease of cacao, and it can infect the tomato Micro-Tom (MT). Typical symptoms are stem swelling and shoot outgrowth, whereas reduction in root biomass is another side effect. We investigated whether the impairment of root growth derives from a hormonal imbalance or sink competition. Intense stem swelling coincided with a reduction in root biomass, predominantly of lateral roots. A few genes involved in hormone metabolism were activated; however, hormonal levels were not altered. Inoculation of the auxin highly-responsive entire genotype maintained the impaired root phenotype. Genes involved in root respiration, carbohydrate, amino acid and cell wall metabolism were repressed, whereas genes linked to water/nitrogen/phosphorous starvation were upregulated. Lower levels of sugars and amino acids suggested carbohydrate deprivation. Less C accumulated in roots of infected MT, but not in the symptomless low-cytokinin MT-transgenic line that overexpresses CYTOKININ OXIDASE-2 ( 35S::AtCKX2 ). We show evidence that the impairment of root development potentially derives from a reduction of photoassimilate supply by the establishment of a strong sink at the shoot symptomatic infection site, rather than hormonal imbalance. We speculate that this impact may contribute to the dramatic decrease in cocoa yields after M. perniciosa invasion.