Verticillium Wilt of Mint in the United States of America

plants Review Verticillium Wilt of Mint in the United States of America Jeremiah K. S. Dung Central Oregon Agricultural Research and Extension Center, Department of Botany and Plant Pathology, Oregon State University, Madras, OR 97741, USA; [email protected] Received: 1 October 2020; Accepted: 10 November 2020; Published: 18 November 2020 Abstract: Verticillium wilt, caused by the fungus Verticillium dahliae, is the most important and destructive disease of mint (Mentha spp.) in the United States (U.S.). The disease was first observed in commercial mint fields in the Midwestern U.S. in the 1920s and, by the 1950s, was present in mint producing regions of the U.S. Pacific Northwest. Verticillium wilt continues to be a major limiting factor in commercial peppermint (Mentha x piperita) and Scotch spearmint (Mentha x gracilis) production, two of the most important sources of mint oil in the U.S. The perennial aspect of U.S. mint production, coupled with the soilborne, polyetic nature of V. dahliae, makes controlling Verticillium wilt in mint a challenge. Studies investigating the biology and genetics of the fungus, the molecular mechanisms of virulence and resistance, and the role of soil microbiota in modulating host-pathogen interactions are needed to improve our understanding of Verticillium wilt epidemiology and inform novel disease management strategies. This review will discuss the history and importance of Verticillium wilt in commercial U.S. mint production, as well as provide a format to highlight past and recent research advances in an effort to better understand and manage the disease. Keywords: Verticillium dahliae; Mentha; soilborne plant pathogens; disease management 1. Mint Production in the United States The genus Mentha L. (family Lamiaceae) encompasses a group of aromatic, mostly perennial herbs that are used in medicines, flavors, and fragrances [1,2]. The aromatic properties of mints are derived from their essential oils, which are produced on leaves in glandular trichomes and extracted using steam distillation [1,3]. Mentha oils are commonly used to flavor foods, gum, confectionaries, dentifrices, and liqueurs, and are also used in pharmaceuticals, cosmetics and aromatherapy products. There are several economically important species and hybrids that are grown commercially for their essential oils, and many more that are grown for local consumption [1]. The cultivation of mint for oil has a long history in the United States, where commercial peppermint (Mentha x piperita L.) production and distillation was first documented in western Massachusetts in the 1790s [1,4]. By the 1830s, production moved into New York and Michigan, where most of the production occurred until the end of the nineteenth century [4]. By the late 1800s, growers were cultivating and distilling oil from native spearmint (Mentha spicata L.), Scotch spearmint (Mentha x gracilis Sole), and ‘Black Mitcham’ peppermint, the latter being a very productive variety of peppermint from England with highly desirable oil qualities [1,4]. The early 20th century saw production shift into the muck soils of Michigan and Indiana, and further west into the Pacific Northwest states of Oregon, Washington, and Idaho, where the majority of U.S. mint oil is currently produced [1,4]. A smaller acreage of mint is also cultivated in the United States to provide dried leaf for teas. Since 2000, the average annual production of peppermint and spearmint (both M. x gracilis and M. spicata) oil in the United States was 2,866,567 kg (on 28,566 ha) and 1,086,852 kg (on 8170 ha), respectively, with a Plants 2020, 9, 1602; doi:10.3390/plants9111602 www.mdpi.com/journal/plants Plants 2020, 9, 1602 2 of 17 Plants 2020, 9, x FOR PEER REVIEW 2 of 18 combinedalso major averageglobal producers annual farmgate of mint of oil, USD but 144,120,150 mint production [5]. India in these and Chinacountries are alsois focused major globalon M. producersarvensis oil of[1] mint. oil, but mint production in these countries is focused on M. arvensis oil [1]. In 1924,1924, aa diseasedisease of of unknown unknown etiology etiology was was observed observed on on a peppermint a peppermint farm farm in Mentha, in Mentha,Michigan Michigan [4,6]. Later[4,6]. Later identified identified as Verticillium as Verticillium wilt, the wilt, disease the soondisease spread soon into spread other into production other production fields in the fields southwest in the areasouthwest of the area state. of In the response, state. In infested response, fields infested in the areafields were in the abandoned area were from abandoned mint cultivation from mint and productioncultivation shiftedand production to central Michigan.shifted to Consequently, central Michigan. Verticillium Consequently, wilt was subsequently Verticillium reported wilt was in Indianasubsequently [7], Oregon reported [8], andin Indiana Washington [7], Oregon [9]. By the[8], mid-twentiethand Washington century, [9]. By Verticillium the mid-twentieth wilt was the century, major productionVerticillium concern wilt was facing the major the U.S. production mint industry concern [4]. facing the U.S. mint industry [4]. 2. Verticillium Wilt of Mint 2.1. Symptoms in Mint Nearly 100 100 years years after after it was it was first first identified identified in peppermint, in peppermint, Verticillium Verticillium wilt continues wilt continues to be the to bemost the important most important and destructive and destructive disease affecting disease commercial affecting commercial mint oil production mint oil in production the United inStates the United[2,10–13] States. Verticillium [2,10–13 ].spp.Verticillium have alsospp. been have reported also been on reported mint in on Brazil, mint inBulgaria, Brazil, Bulgaria, Canada, Canada, Egypt, Egypt,Venezuela, Venezuela, and Zimbabwe and Zimbabwe [14,15], but [14 the,15], disease but the is diseaseof primary is of importance primary importance in U.S. mint inproduction. U.S. mint production.Two of the three Two major of the threecultivars major of mint cultivars grown of mintin the grown U.S., ‘Black in the U.S.,Mitcham’ ‘Black pepperm Mitcham’int peppermint and Scotch andspearmint, Scotch are spearmint, highly susceptible are highly susceptible to Verticillium to Verticillium wilt, while wilt, native while spearmint native spearmintis moderately is moderately to highly toresistant highly [16,17] resistant. Cornmint, [16,17]. Cornmint, which is the which major is theMentha major oilMentha crop inoil India crop and in IndiaChina, and exhibits China, moderate exhibits moderateresistance resistanceto Verticillium to Verticillium wilt [17]. wilt [17]. Symptoms of Verticillium wiltwilt in mint can vary depending on the Mentha species species that that is is infected, infected, the stage of the crop,crop, andand environmentalenvironmental conditions. While While symptoms do do not not often often follow follow a a regular progression, inin most most cases cases symptoms symptoms begin begin in the apicalin the meristem, apical mer namelyistem, the namely asymmetric the developmentasymmetric ofdevelopment leaves that of appear leaves to that twist appear and curl to twist into aand crescent curl into shape a crescent (Figure1 shapeA,B). Internodes(Figure 1A, canB). beInternodes shorter, resultingcan be shorter, in the resulting bunching in of the upper bunching leaves of and upper/or stunted leaves and/or plants (Figurestunted1 C).plants New (Fig growthure 1C can). New be chloroticgrowth can or be exhibit chlorotic reddening or exhibit or bronzingreddening (Figure or bronzing2A,B). (Fig As theure disease2A,B). As progresses the disease in progresses peppermint, in chlorosispeppermint, develops chlorosis at the develops base of theat plantthe base and of progresses the plant upwards, and progresses resulting upwards, in defoliation resulting of lower in leaves;defoliation in spearmint, of lower leaves; chlorosis in mayspearmint, be more chlorosis pronounced may be and more affect pronounced the whole plant.and af Symptomsfect the whole can occurplant. onSymptoms one or a can few occur stems on or one the or entire a few plant stems depending or the entire on the plant extent depending and duration on the ofextent infection and (Figureduration2C). of infection Infected stems(Figure may 2C). exhibit Infected xylem stems discoloration. may exhibit Susceptiblexylem discoloration. mints that Susceptible succumb tomints the diseasethat succumb eventually to the exhibit disease wilt eventually and senesce exhib prematurelyit wilt and senesce [18]. Flowering prematurely or other [18] stresses. Flowering can expediteor other wiltstresses and can plant expedite senescence. wilt and Over plant time, senescence. foci of dead Over plants time, develop foci of (Figuredead plants2D) and develop coalesce, (Fig leavingure 2D) largeand coalesce, areas of leaving mint fields large bare areas (Figure of mint2E). fields bare (Figure 2E). A B C Figure 1. (A) Twisted, curled, and crescent crescent-shaped-shaped leaves of peppermint and and ( (B)) Scotch Scotch spearmint spearmint.. (C) Verticillium wiltwilt cancan causecause severesevere stuntingstunting inin susceptiblesusceptible cultivars.cultivars. 2.2. Economic Impacts Economic losses due to Verticillium wilt of mint are both primary and secondary [6]. Primary losses are realized as reduced oil yields caused by stunting, defoliation, or early senescence. The Plants 2020, 9, 1602 3 of 17 Plants 2020, 9, x FOR PEER REVIEW 4 of 18 A B C D E F Figure 2.2. (A(A)) Chlorosis Chlorosis

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