Panama disease or Fusarium wilt is caused by the soil-borne fungus Fusarium oxysporum f.sp. cubense (Foc), and was first described in Australia in 1874 (Bancroft, 1876). The fungus penetrates the roots and from there colonizes the vascular system of the banana plant. Together with the plant responses, this results in occlusion of the xylem vessels which causes wilting and eventually death of infected plants (Guo et al., 2014). The decimation of susceptible “Gros Michel” bananas that were grown in large-scale monoculture plantations in Central America during the 1900s earned Fusarium wilt its reputation as a pathogen of global significance. Losses of “Gros Michel” were first recognized in Central America (Costa Rica and Panama) in 1890, and were soon reported in Africa, the Caribbean, and South America (Ploetz, 2015). The Fusarium wilt epidemic was caused by a set of Foc strains that are collectively called Race 1 and decimated the large-scale monocultures of “Gros Michel” on which the banana industry in America relied. No effective control methods were found other than replacing “Gros Michel” with resistant “Cavendish” bananas in Central America during the 1960s. This replacement has been highly successful to quench the Fusarium wilt epidemic that was caused by Foc Race 1 strains. Since then, “Cavendish” production expanded into large global monocultures, which are evidently prone to disease threats, including black Sigatoka and Panama disease (Ordoñez et al., 2015b; Arango Isaza et al., 2016; Diaz-Trujillo et al., 2018). However, this has not resulted in global research efforts to neutralize these problems. Therefore, another genetic lineage of Foc [vegetative compatibility group (VCG) 01213], colloquially called Tropical Race 4 (Foc TR4), which originates from Indonesia and affects many banana varieties, including those belonging to the “Cavendish” group, has now developed into a global threat (Ordoñez et al., 2015b). It has spread to five Asian “Cavendish”-producing countries and Australia, and was recently also discovered in the Middle East, the Indian subcontinent and Africa (García-Bastidas et al., 2014; Ordonez et al., 2015a; Ploetz et al., 2015; Promusa, 2016). Therefore, the global banana industry is under serious threat by this soil-borne fungal disease (Ploetz and Churchill, 2011; Pocasangre et al., 2011; Shabani et al., 2014; Ordoñez et al., 2015b), and its recent rapid spread has raised international concerns with regard to future food security in the tropics and sustainability of the international banana trade that is nearly exclusively based on “Cavendish” clones (D'hont et al., 2012; FAO, 2014). Currently, “Cavendish” clones comprise 15% of the global banana production but they are increasingly gaining importance for domestic markets. Presently, they occupy ~40% (Ploetz et al., 2015) of the total global area. Clearly, this comes with a huge risk for a pandemic as these clones are susceptible to Foc TR4. The vegetative propagation of planting material and a lack of diversification efforts over the last century have increased the genetic vulnerability of the crop to unacceptable levels, which threatens food security. This urges for international, regional, and local measures aimed at prevention and management of this destructive disease (Ploetz, 2015).

The biological complexity of soil-borne diseases—with surviving propagules that remain viable for decades—and taking into account the historical track-record of Foc (Li et al., 2013), demonstrates that disease management has proven to be difficult (Ploetz, 2015). Hence, prevention is currently the major strategy to avoid new Foc TR4 incursions. In 1967, Foc TR4 surfaced in Taiwan, supposedly after introduction of infected plants from Sumatera, Indonesia (Su et al., 1977; Hwang and Ko, 2004). From there, it has disseminated likely into the Chinese province of Fujian, and then gradually to Guangdong, Guangxi, Hainan and finally in 2009 to Yunnan (Sun et al., 1978; Su et al., 1986; Hwang and Ko, 2004; Qi et al., 2008; Buddenhagen, 2009; Li et al., 2013). The expansion of Foc TR4 was facilitated by new large scale “Cavendish” production practices across this area along with limited awareness and lacking quarantine measures. The cultivation of “Cavendish” now shifts to Laos, Myanmar, Vietnam, and other countries in the Greater Mekong Subregion because of limited suitable land for banana production to meet the increasing market demand. During a survey in Vietnam, Laos, and Myanmar in March and May 2016 we observed the presence of Fusarium wilt in “Cavendish” plantations. Here, we provide details on the regional and international expansion of Foc TR4, which is worrisome as it threatens both food security and the international trade (Ordonez et al., 2015a; Ploetz et al., 2015; Mostert et al., 2017).

This study provides the earliest collected records of Foc TR4 in Vietnam and Laos and its first report in Myanmar. Recently, Mostert et al. (2017) denied the presence of Foc TR4 in Vietnam, Cambodia, and Thailand based on samples that were collected a decade ago, but (Chittarath et al., 2017; Hung et al., 2017) confirmed it in Vietnam and Laos. Our genome analyses revealed a set of SNPs that we used to further analyze the genetic diversity of Foc TR4 strains. Isolates from Vietnam, Laos, and Myanmar are genetically closely related and resemble the Foc TR4 strain from Yunnan. Furthermore, we demonstrate genetic association between the Foc TR4 strains from Pakistan and the Philippines as well as between the strains from Lebanon and Jordan. Although Foc TR4 is an asexually reproducing fungus which therefore shows a very strong linkage disequilibrium, clonal evolution does occur as evidenced by genetic clustering which enabled our biogeographical analysis (Tibayrenc and Ayala, 2012).

Recently, we demonstrated that the globally disseminating Foc TR4 strain represents essentially a single clone (Ordoñez et al., 2015b). Hence, it was difficult to unveil the origin of new incursions. However, we identified 251 high value SNPs that also after filtering elucidate basic associations between the here identified Foc TR4 strains. Such analyses were recently also used to reveal the dissemination of the quarantine pathogen Xylella fastidiosa in olive trees (Loconsole et al., 2014). Here, such a phylogeography approach provides initial evidence that Foc TR4 in Laos, Vietnam, and Myanmar was likely introduced from China. This supports the circumstantial evidence of ongoing Foc TR4 epidemics on “Cavendish” plantations in these countries and adjacent Chinese provinces, which were developed by Chinese banana entrepreneurs. The SNP analyses also revealed that the Foc TR4 strains from the Philippines and from Pakistan are closely related. Since Foc TR4 was diagnosed in the Philippines in 2005 (Molina et al., 2009) and is currently omnipresent in Mindanao, the recent incursion in Pakistan (Ordonez et al., 2015a) seems to originate from the Philippines. Similarly, the phylogeography data set indicates that the Foc TR4 incursions in Lebanon and Jordan are associated (García-Bastidas et al., 2014).

The introduction of large scale “Cavendish” monocultures in the GMS resulted in displacement of local peoples, disputes on landownership and also resulted in a rapid decrease in forest area, which challenges ecological stability (Rerkasem et al., 2009; Yoshida et al., 2010; Friis and Nielsen, 2016). We demonstrate that it also facilitated yet another expansion of Foc TR4. The dissemination of Foc TR4 in China upon the initial introduction from Taiwan is not well documented. Evidently, low awareness among banana growers and industry stakeholders has resulted in an almost unlimited movement of banana suckers, contaminated nursery soils, and farming equipment as well as the use of contaminated surface irrigation water. Our phylogeography approach indicates that these practices and the mobility of banana stakeholders may have contributed to the expansion of Foc TR4 (Drenth and Guest, 2016).

Similar to the previous Panama disease epidemic in “Gros Michel” caused by Foc Race 1 the lag phase of the current epidemic is substantial as the first occurrence of Foc TR4 was observed 50 years ago in Taiwan (Su et al., 1977, 1986; Hwang and Ko, 2004). However, the track-record of Fusarium wilt epidemics in banana is unparalleled in botanical epidemiology (Ploetz, 2015), and hence we should not underestimate the impact of the current Foc TR4 pandemic on food and fruit production. Despite numerous efforts to alert and mobilize the banana sector for enhanced quarantine practices, we observe a continuous dissemination of Foc TR4 (García-Bastidas et al., 2014; Ordonez et al., 2015a; Ploetz et al., 2015; Promusa, 2016; Chittarath et al., 2017; Hung et al., 2017). High resolution phylogeography may increase overall awareness and responsibility among banana stakeholders to prevent the further dissemination of Foc TR4.

S-JZ: Conceived the experiments, collected the samples, analyzed the data, wrote the paper; FG-B: Analyzed the samples, wrote the paper; XL, LZ, TB, SX, KY, HL, YY, and LY: Collected the samples, analyzed the data; GF: Collected the samples, analyzed the data, wrote the paper; HN, BD, and AK: Ensured visits to banana farms, collected samples, organized permits; AD: Provided training, analyzed the data, wrote the paper; MS and HM: Analyzed the data, wrote the paper; GK: Conceived the experiments, organized the sampling, analyzed the data, wrote the paper.