Phylogeny and genetic diversity of the banana Fusarium wilt pathogen Fusarium oxysporum f. sp. cubense in the Indonesian centre of origin

Abstract

Fusarium oxysporum f. sp. cubense (Foc), the causal agent of Fusarium wilt or Panama disease on banana, is one of the major constraints in banana production worldwide. Indonesia is the centre of origin for wild and cultivated bananas, which likely co-evolved with Foc. This study explored the widest possible genetic diversity of Foc by sampling across Indonesia at 34 geographically and environmentally different locations in 15 provinces at six islands. This resulted in a comprehensive collection of ∼200 isolates from 40 different local banana varieties. Isolates were identified and assessed using sequence analysis of the translation elongation factor-1alpha (tef1), the RNA polymerase II largest subunit (rpb1), and the RNA polymerase II second largest subunit (rpb2). Phylogenetic analyses of these genes allowed the identification of 180 isolates of Fusarium oxysporum f. sp. cubense (Foc), and 20 isolates of the Fusarium fujikuroi species complex (FFSC), the Fusarium incarnatum-equiseti species complex (FIESC), and the Fusarium sambucinum species complex (FSSC). Further analyses, incorporating a worldwide collection of Foc strains, revealed nine independent genetic lineages for Foc, and one novel clade in the Fusarium oxysporum species complex (FOSC). Selected isolates from each lineage were tested on the banana varieties Gros Michel and Cavendish to characterise their pathogenicity profiles. More than 65 % of the isolates were diagnosed as Tropical Race 4 (Foc-TR4) due to their pathogenicity to Cavendish banana, which supports the hypothesis that Foc-TR4 is of Indonesian origin. Nine independent genetic lineages for Foc are formally described in this study. This biodiversity has not been studied since the initial description of Foc in 1919. This study provides a detailed overview of the complexity of Fusarium wilt on banana and its diversity and distribution across Indonesia.

Fungal clones win the battle, but recombination wins the war

“…Organisms known only from their mitotic stage, such as Fusarium oxysporum f.sp. cubense tropical race 4 of banana (recently renamed F. odoratissimum) (Ordonez et al 2015;Maryani et al 2019), may be regarded as evidence of success without sexual reproduction. But the origin of these successful genotypes remains unanswered.…”

A loop‐mediated isothermal amplification (LAMP) assay based on unique markers derived from genotyping by sequencing data for rapid in planta diagnosis of Panama disease caused by Tropical Race 4 in banana

“…Currently in bananas, the emerging TR4 strain causing fusarium wilt may potentially cause a pandemic (Butler, 2013;Ord oñez et al, 2015;Stokstad, 2019) that surpasses the first outbreak of the disease in Latin America (Ploetz, 2015a). Tropical race 4 belongs to F. odoratissimum and is omnipresent in Indonesia (Maryani et al, 2019). Since its first encounter with Cavendish in Taiwan (Molina et al, 2009;Ploetz, 2015a) TR4 has disseminated within and outside South-East Asia (Garc ıa-Bastidas et al, 2014;Ord oñez et al, 2016;Chittarath et al, 2017;Hung et al, 2017;Mostert et al, 2017;Zheng et al, 2018) and recently surfaced in Colombia (Stokstad, 2019).…”

“…cubense race 1 strains that caused the previous epidemic as seven individual Fusarium spp. (Maryani et al , ). However, the current epidemic in Cavendish plantations as well as in manifold local banana varieties is caused by the so‐called tropical race 4 (TR4; previously Fusarium oxysporum f. sp.…”

“…cubense race 1 strains that caused the previous epidemic as seven individual Fusarium spp. (Maryani et al, 2019).…”

“…However, the current epidemic in Cavendish plantations as well as in manifold local banana varieties is caused by the so-called tropical race 4 (TR4; previously Fusarium oxysporum f. sp. cubense tropical race 4) that belongs to the new species Fusarium odoratissimum, and causes devastation in many producing areas (Ploetz, 2006(Ploetz, , 2015a(Ploetz, ,2015bGarc ıa-Bastidas et al, 2019;Maryani et al, 2019). Unlike in the past, there is no commercially acceptable banana germplasm to replace Cavendish (Ploetz, 2015b) other than the widely promoted Cavendish somaclones that are less susceptible to TR4 (Hwang & Ko, 2004).…”