The Emergence of Fusarium oxysporum f. sp. apii Race 4 and Fusarium oxysporum f. sp. coriandrii Highlights Major Obstacles Facing Agricultural Production in Coastal California in a Warming Climate: A Case Study

Abstract

Currently, Fusarium oxysporum f. sp. apii (Foa) race 4 in celery and F. oxysporum f. sp. coriandrii (Foci) in coriander have the characteristics of emerging infectious plant diseases in coastal southern California: the pathogens are spreading, yield losses can be severe, and there are currently no economical solutions for their control. Celery, and possibly coriander, production in these regions is are likely to have more severe disease from projected warmer conditions in the historically cool, coastal regions. Experimental evidence shows that Foa race 4 causes much higher disease severity when temperatures exceed 21°C. A phylogenomic analysis indicated that Foa race 4, an older, less virulent, and uncommon Foa race 3, and two Foci are closely related in their conserved genomes. These closely related genotypes are somatically compatible. Foa race 4 can also cause disease in coriander and the two organisms readily form “hetero” conidial anastomosis tubes (CAT), further increasing the likelihood of parasexual recombination and the generation of novel pathotypes. A horizontal chromosome transfer event likely accounts for the difference in host range between Foci versus Foa races 4 and 3 because they differ primarily in one or two accessory chromosomes. How Foa race 4 evolved its hyper-virulence is unknown. Although the accessory chromosomes of Foa races 3 and 4 are highly similar, there is no evidence that Foa race 4 evolved directly from race 3, and races 3 and 4 probably only have a common ancestor. Foa race 2, which is in a different clade within the Fusarium oxysporum species complex (FOSC) than the other Foa, did not contribute to the evolution of race 4, and does not form CATs with Foa race 4; consequently, while inter-isolate CAT formation is genetically less restrictive than somatic compatibility, it might be more restricted between FOSC clades than currently known. Other relatively new F. oxysporum in coastal California include F. oxysporum f. sp. fragariae on strawberry (Fof). Curiously, Fof “yellows-fragariae” isolates also have similar core genomes to Foa races 4 and 3 and Foci, perhaps suggesting that there may be core genome factors in this lineage that favor establishment in these soils.

Tolerance Evaluation of Celery Commercial Cultivars and Genetic Variability of Fusarium oxysporum f. sp. apii

“…According to reports by Epstein et al [17], the genetic improvement of celery cultivars has been carried out based on races 2 and 4, considered the most virulent races in the United States and other latitudes. After the establishment of race 2 in California, it was transported on infested seed to other states and countries such as Canada, Japan, and Argentina [17].…”

“…According to reports by Epstein et al [17], the genetic improvement of celery cultivars has been carried out based on races 2 and 4, considered the most virulent races in the United States and other latitudes. After the establishment of race 2 in California, it was transported on infested seed to other states and countries such as Canada, Japan, and Argentina [17]. The low levels of resistance of seed cultivars imported to Costa Rica to race 3 may be due to the fact that most of the genetic improvement on celery cultivars has been conducted based on races 2 and 4 tolerance.…”

“…apii, have been reported as the primary pathogen in celery and Tithonia rotundifolia, and as a secondary pathogen in a broad diversity of hosts, including cotton (Gossypium barbadense and G. arboretum), garden pea (Pisum sativum), sicklepod (Cassia tora) and eggplant (Solanum melongena) [16]. In recent studies, it has been demonstrated that Foa race 4 can cause disease in coriander (Coriandrum sativum) [17,26]. Additionally, it has been reported that coriander is a secondary host to Foa races 2 and 3, but these races are reported as less virulent than race 4 [13].…”

“…It is common at temperatures above 22 • C [5] and has been spreading within California since its discovery. Currently, race 4 cannot be controlled via either host resistance or chemical methods that reduce the pathogen abundance in infested soils [17].…”

Apium graveolens PI 181714 is a source of resistance to Fusarium oxysporum f. sp. apii race 4 in celery (A. graveolens var. dulce)

“…California is the major producer of celery in the United States, with production of 744 000 tonnes in 2018 (USDA, 2020). Foa race 4 ( Foa R4), a new fungal pathogen of celery, was first reported in Camarillo, California, USA in 2017 (Epstein et al, 2017; Epstein et al, 2022); it is comparatively unrelated to Foa R2 (Henry et al, 2020). FoaR4 causes Fusarium wilt of celery, which can cause complete crop loss, particularly when temperatures are 22°C and above (Kaur et al, 2022).…”