Connecting the rots: Relating past and current tomato diseases of varied impact to species, haplotypes and somatic compatibility groups in the <i>Fusarium solani</i> Species Complex (FSSC)

Here we place isolates from a serious emerging disease of California tomato associated with <i>Fusarium solani</i> Species Complex (FSSC) in a taxonomic/clonal framework of global and historical FSSC-associated tomato disease. Standard FSSC sequence markers (<i>tef1a, rDNA, rpb2</i>) resolved at least four closely related modern species as tomato pathogens globally: <i>F. noneumartii, F. martii, F. falciforme</i> and <i>F. solani-melongenae</i>. Based on sequence analysis, somatic compatibility grouping and inoculation studies, our work connects a single <i>F. noneumartii</i> clone in California (SCG FN-1) to modern California isolates (2017-2020) associated with serious symptoms (stem rot, vine decline) and impacts (fruit damage and loss). Historical (1996-2001) California tomato foot rot isolates from California are also FN-1, and show severe virulence and yield impacts similar to those of modern FN-1 isolates, indicating that this virulent pathogen was present at least twenty years prior to the modern severe outbreak. Discovery of a single moderately virulent California <i>F. martii</i> clone (SCG FM-1) marks the first connection between <i>F. martii</i> and plant disease. Clonally diverse <i>F. falciforme</i> isolates from California tomato, which did not cause severe symptoms, represent clonally diverse haplotypes/SCGs different from <i>F. falciforme</i> pathogens from Mexico, and a putative Australia foot rot pathogen from 1982. <i>tef1a</i> sequence comparisons demonstrate that <i>F. noneumartii</i> and <i>F. martii</i> have multicontinental distributions associated with many plant hosts, and show similarity between FN-1 and 2010 foot rot isolates from Japan. This clarification of global diversity, distribution and biology of FSSC tomato pathogens provides a new framework for disease management and diagnosis.