Establishment of Basic Compatibility Through Pathogen Sulfur Scavenging Is Essential for Laurel Wilt Disease Development.

Abstract

Invasive, lethal tree diseases continue to have devastating effects on forest ecology, commercial timber production, the horticultural trade, and agriculture production. Laurel wilt, caused by the recently introduced fungus Harringtonia lauricola, is one such lethal disease threatening both native ecosystems and avocado production. Previous transcriptomic analyses determined that a massive upregulation of pathogen genes involved in the uptake and metabolism of sulfur compounds occurs during host colonization. The creation of a loss-of-function mutant for pathogen-encoded HlCys3, a bZIP transcriptional regulator of alternative sulfur utilization, abolished colonization and disease. This phenotype was complemented genetically and chemically by reintroduction of the wild-type Hlcys3 gene in the mutant and by exogenously supplying methionine during mutant infection, respectively. These findings establish pathogen sulfur metabolism as a basic compatibility factor for this disease. The role of basic compatibility was further explored by establishing the temporal-spatial and morphological dynamics of tree host colonization by H. lauricola in comparison with the nonpathogenic species H. aguacate. The nonpathogen was able to colonize Lauraceae hosts at and adjacent to the inoculation zone, similarly to the pathogen, but was unable to systemically colonize trees. Differences in these colonization patterns were not associated with the timing or magnitude of tylosis development at the infection point. These findings indicate that basic compatibility for niche occupation must be coupled with specific compatibility factors for systemic colonization and symptom development. Determining the universality of these findings in other vascular tree wilting diseases may suggest strategies for mitigating tree mortality in ecosystems and agriculture. [Formula: see text] Copyright © 2026 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.