Evidence for high gene flow, nonrandom mating, and genetic bottlenecks of Ganoderma boninense infecting oil palm (Elaeis guineensis Jacq.) plantations in Malaysia and Indonesia

ABSTRACT

Ganoderma boninense, the causal agent of basal stem rot (BSR) disease, has been recognized as a major economic threat to commercial plantings of oil palm (Elaeis guineensis Jacq.) in Southeast Asia, which supplies 86% of the world’s palm oil. High genetic diversity and gene flow among regional populations of 417 G. boninense isolates collected from Sabah, Sarawak, and Peninsular Malaysia (Malaysia) and Sumatra (Indonesia) were demonstrated using 16 microsatellite loci. Three genetic clusters and different admixed populations of G. boninense across regions were detected, and they appeared to follow the spread of the fungus from the oldest (Peninsular Malaysia and Sumatra) to younger generations of oil palm plantings (Sabah and Sarawak). Low spatial genetic differentiation of G. boninense (F_ST = 0.05) among the sampling regions revealed geographically nonrestricted gene dispersal, but isolation by distance was still evident. Analysis of molecular variance (AMOVA) confirmed the little to no genetic differentiation among the pathogen populations and the three genetic clusters defined by STRUCTURE and minimum spanning network. Despite G. boninense being highly outcrossing and spread by sexual spores, linkage disequilibrium was detected in 7 of the 14 populations. Linkage disequilibrium indicated that the reproduction of the fungus was not entirely by random mating and genetic drift could be an important structuring factor. Furthermore, evidence of population bottleneck was indicated in the oldest oil palm plantations as detected in genetic clusters 2 and 3, which consisted mainly of Peninsular Malaysia and Sumatra isolates. The population bottleneck or founding event could have arisen from either new planting or replanting after the removal of large number of palm hosts. The present study also demonstrated that migration and nonrandom mating of G. boninense could be important for survival and adaptation to new palm hosts.

KEYWORDS:

• Basal stem rot
• evolutionary potential
• fungal pathogen
• genetic structure
• genotyping

ACKNOWLEDGMENTS

We greatly appreciate the field and laboratory assistances provided by the Molecular and Microbiology Research Division, Sarawak Tropical Peat Research Institute, and by Mr. Chua Kian Hong (Group Plantation Controller, Sarawak Oil Palm Bhd.). We thank also Mr. Bacho A. Sappe (AAR’s Sabah substation) and Prof. Dr. Chong Khim Phin (University of Sabah Malaysia) for providing laboratory assistances in Sabah. Messrs. Ismail Hassim, Muhammad Al Qayyum Hassam Basri (AAR’s Pests and Diseases [P&D]) and P&D members of PT Applied Agricultural Resources Indonesia coordinated the Ganoderma trial census and basidiocarp sampling in Peninsular Malaysia and Sumatra throughout the years. We are grateful to Mr Chew Poh Soon, who has provided invaluable insights into the Ganoderma disease in oil palm and critical review of the manuscript.

DISCLOSURE STATEMENT

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/00275514.2022.2118512

Additional information

Funding

We gratefully acknowledge Applied Agricultural Resources Sdn. Bhd.’s (AAR) principals, Boustead Plantations Berhad, and Kuala Lumpur Kepong Berhad, for their unwavering support given to our research project that generated the data presented here and their permission to publish this article. The funding from J. William Fulbright Foreign Scholarship Board, which was supported by the U.S. Department of State Bureau of Educational and Cultural Affairs and the Malaysian-American Commission on Educational Exchange, had permitted, in part, the research travel expenses to the University of Tennessee (UT), Knoxville, Tennessee, for Dr. Wong. We thank UT AgResearch and Department of Entomology and Plant Pathology, University of Tennessee, for hosting Dr. Wong under the Fulbright Professional Exchange Program (January to March 2019).