How megadrought causes extensive mortality in a deep‐rooted shrub species normally resistant to drought‐induced dieback: The role of a biotic mortality agent

• Published in: Plant, cell and environment cell and environment, 2024-04, Vol.47 (4), p.1053-1069
• Main Authors: Aguirre, Natalie M., Ochoa, Marissa E., Holmlund, Helen I., Palmeri, Gabriella N., Lancaster, Emily R., Gilderman, Gina S., Taylor, Shaquetta R., Sauer, Kaitlyn E., Borges, Adriana J., Lamb, Avery N. D., Jacques, Sarah B., Ewers, Frank W., Davis, Stephen D.
• Format: Article
• Language: English
• Subjects: Botryosphaeria; Botryosphaeria dothidea; Carbon; Chaparral; Dieback; Drought; drought‐induced mortality; Endophytes; fungus; Malosma laurina; Mortality; Mountains; Plants (botany); predisposition; Stems; Water deficit; Water transport; Xylem
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14768

Southern California experienced unprecedented megadrought between 2012 and 2018. During this time, Malosma laurina, a chaparral species normally resilient to single‐year intense drought, developed extensive mortality exceeding 60% throughout low‐elevation coastal populations of the Santa Monica Mountains. We assessed the physiological mechanisms by which the advent of megadrought predisposed M. laurina to extensive shoot dieback and whole‐plant death. We found that hydraulic conductance of stem xylem (Ks, native) was reduced seven to 11‐fold in dieback adult and resprout branches, respectively. Staining of stem xylem vessels revealed that dieback plants experienced 68% solid‐blockage, explaining the reduction in water transport. Following Koch's postulates, persistent isolation of a microorganism in stem xylem of dieback plants but not healthy controls indicated that the causative agent of xylem blockage was an opportunistic endophytic fungus, Botryosphaeria dothidea. We inoculated healthy M. laurina saplings with fungal isolates and compared hyphal elongation rates under well‐watered, water‐deficit, and carbon‐deficit treatments. Relative to controls, we found that both water deficit and carbon‐deficit increased hyphal extension rates and the incidence of shoot dieback. Summary statement We conclude that the ultimate cause of mortality of Malosma laurina in field populations was megadrought and that the proximal cause of mortality was the transition of endemic Botryosphaeria dothidea to an opportunistic pathogen that amplified protracted water stress through physical blockage of xylem water transport.