Journal of Plant Pathology (2016), 98 (3), 379-404 Edizioni ETS Pisa, 2016 379

Offered Review

PHYTOPLASMA DISEASES OF MEDICINAL AND AROMATIC PLANTS

C. Marcone1, M.G. Bellardi2 and A. Bertaccini2

1 Department of Pharmacy, University of Salerno, Via Giovanni Paolo II, 132, I-84084 Fisciano (Salerno), Italy 2 Department of Agricultural Science, Alma Mater Studiorum - University of Bologna, Viale G. Fanin, 42, I-40127 Bologna, Italy

SUMMARY INTRODUCTION

Medicinal and aromatic plants include a broad array Medicinal and aromatic plants include a broad array of of wild and cultivated plants which contain many biolog- wild and cultivated plants which provide raw materials for ically-active compounds, known as phytochemicals, that medicines, nutraceuticals, perfumes, flavors and cosmetics. are of great interest for their ability to promote human These plants contain many biologically-active compounds, and animal health. The present review provides a litera- namely secondary metabolites, which are known as phyto- ture overview of phytoplasma diseases affecting medicinal chemicals that are of great interest for their ability to pro- and aromatic plants, with an emphasis on phytoplasma mote human and animal health. Currently, the demand for taxa associated. An overview of studies that examined the medicinal and aromatic plants and their derived products effect of phytoplasma infections on phytochemical con- is greatly increasing. Among the several diseases affecting tent and other secondary metabolites of affected plants medicinal and aromatic plants, there are yellows, witches’ is also included. Phytoplasma diseases of medicinal and broom and decline diseases, associated with phytoplasma aromatic plants occur worldwide; however, the majority presence, which severely impair productivity, phytochemi- of reports are from Europe and southeastern Asian coun- cal content and longevity of affected plants. tries. These diseases affect plant species belonging to over Phytoplasmas are a large group of plant-pathogenic 70 families, mostly to Apiaceae and Asteraceae. They dif- wall-less bacteria associated with diseases in more than a fer considerably in geographic distribution and size of the thousand plant species worldwide. They are transmitted various taxonomic groups and subgroups of the associ- from plant to plant by phloem-feeding homopteran in- ated phytoplasmas. Subgroup 16SrI-B phytoplasmas are sects, mainly leafhoppers and planthoppers, less frequently the prevalent agents occurring mainly in Europe, North psyllids, in a persistent, propagative manner (Weintraub America and Asia. Phytoplasma presence induces changes and Beanland, 2006). Most of the phytoplasma host plants in the amount and composition of secondary metabolites are angiosperms in which a wide range of specific and in diseased plants in which, however, the concentrations non-specific symptoms are induced (Seemüller et al., of valuable phytochemicals are greatly affected. An excep- 2002; Bertaccini et al., 2014). Specific symptoms include tion is represented by phytoplasma diseases of periwinkle virescence, phyllody, big bud, flower proliferation and in which an accumulation of pharmaceutically impor- other flower abnormalities, resulting in sterility, witches’ tant compounds occurs upon phytoplasma infections. brooms, rosetting, internode elongation and etiolation, Prospects for future research are presented and critically shortened internodes, off-season growth, and brown dis- discussed. coloration of phloem tissue. Less specific and non-specific symptoms which are most often common in woody plants, Keywords: ‘Candidatus Phytoplasma’ species, 16Sr include foliar yellowing and reddening, small leaves, leaf group/subgroups, phytochemicals, secondary metabolites, roll, leaf curl, vein clearing, vein enlargement, vein necro- symptomatology, yellows diseases. sis, premature autumn coloration, premature defoliation, poor terminal growth, sparse foliage, die-back, stunting, and decline. Since these prokaryotes live and multiply in functional phloem sieve tube elements, they mainly impair their func- tionality. The inhibition of phloem transport along with other impaired physiological functions including reduced photosyntesis, altered secondary metabolism and plant hormone imbalance explain the symptoms exhibited by Corresponding author: C. Marcone phytoplasma-infected plants (Lepka et al., 1999; Tan and Fax: +39.089.969602 E-mail: [email protected] Whitlow, 2001; Bertamini et al., 2002; Choi et al., 2004; 380 Phytoplasma diseases Journal of Plant Pathology (2016), 98 (3), 379-404

Endeshaw et al., 2012; Ding et al., 2013; Vitali et al., 2013). the prevalent agents occurring mainly in Europe, North However, the mechanisms by which phytoplasmas induce America and Asia. Phytoplasmas of 16SrXII-A subgroup disease in plants and the different reactions of the host with a few exceptions, e.g., Artemisia scoparia witches’ plants are still poorly understood. Several plant host genes, broom and Salvia miltiorrhiza red leaf agents, both oc- which are differentially expressed upon phytoplasma in- curring in China, as well as phytoplasmas of 16SrX and fections, were identified. These include genes involved in 16SrXX groups are restricted to Europe, whereas phyto- phytohormone activity, photosynthesis, carbohydrate and plasmas of the 16SrII group are prevalent in Asia and Aus- lipid metabolism, amino acid transport, and secondary tralia. Also, phytoplasmas of 16SrIV, 16SrXIII, 16SrXV, metabolite biosynthesis genes (Pracros et al., 2006; Chen 16SrXXIX, 16SrXXX and 16SrXXXII groups have only and Lin, 2011; Landi and Romanazzi, 2011; Albertazzi et been identified in diseased medicinal and aromatic plants al., 2009; Hren et al., 2009a, 2009b; Ding et al., 2013). In in Asia and South America. Like other phytoplasma dis- addition, a considerable number of genes that are likely eases, a number of diseases of medicinal and aromatic to play major roles in phytoplasma-host interactions are plants are associated each with genetically different phy- known from the complete genome sequences of the phyto- toplasmas, up to seven in some instances, which induce plasmas that have been determined to date. Among these, similar symptoms in a given plant host and occur either there are genes encoding surface membrane proteins and within the same geographic areas or different continents. effector (virulence) proteins (Hoshi et al., 2009; MacLean Among these, there are dill yellows, celery yellows, peri- et al., 2011; Sugio et al., 2011a, 2011b; Kube et al., 2012; winkle yellows and phyllody, cirsium yellows, purple cone- Neriya et al., 2014). flower yellows, dandelion yellows, alfalfa witches’ broom, Taxonomically, phytoplasmas are placed in the class mallow yellows, Chinaberry yellows, myrtle yellows, rose Mollicutes and are currently classified within the provi- yellows, and grapevine yellows. The remaining diseases of sional genus ‘Candidatus Phytoplasma’ based primarily medicinal and aromatic plants are attributed to one or a on 16S rDNA sequence analysis (IRPCM, 2004; Martini few phytoplasmas (Table 1). Also, a given plant host may et al., 2014). Approximately 33 major phylogenetic groups be singly or doubly or multiply infected with distinctly dif- were identified within the phytoplasma clade (Bertaccini ferent phytoplasmas. The latter phenomenon is common et al., 2014). This figure is broadly in accordance with the in perennial plants, e.g., Spanish broom, eucalypt, myrtle, number of phytoplasma groups established by restric- olive, pomegranate, rose, rosemary, lavender, whose long tion fragment length polymorphism (RFLP) analysis of life spans provide opportunities to be infected by insect PCR-amplified rDNA (Lee et al., 1998, 2000; Seemüller vectors carrying various phytoplasmas (Table 1). In many et al., 1998, 2002). Within the majority of the phytoplasma instances, wild medicinal and aromatic plants listed in groups, several distinct subgroups have been delineated, Table 1 act as alternative hosts for phytoplasmas associ- based on the RFLP analysis of 16S rDNA sequences (Lee ated with economically important diseases of vegetable, et al., 1998, 2007). To date, 40 ‘Candidatus Phytoplasma’ ornamental, and fruit crops. These include field bindweed, species have been formally described (IRPCM, 2004; hedge bindweed, nettle, and lavender that are alternative Bertaccini et al., 2014; Davis et al., 2016; Fernández et al., hosts of the “stolbur” phytoplasma, pot marigold, dandeli- 2016; Šafářová et al., 2016). on, broad leaf plantain, wild carrot, daisy, creeping thistle, This review provides a literature overview of phyto- prickly lettuce and wild radish, which are alternative hosts plasma diseases affecting medicinal and aromatic plants of aster yellows phytoplasmas, howthorn and blackthorn, examining also the effect of phytoplasma presence on the alternative hosts of phytoplasmas of the 16SrX group in phytochemical content of affected plants. which phytoplasmas infecting fruit trees are also enclosed.

PHYTOPLASMA DISEASES OF MEDICINAL AND EFFECT OF PHYTOPLASMAS ON PHYTOCHEMICAL AROMATIC PLANTS CONTENT AND OTHER SECONDARY METABOLITES IN AFFECTED PLANTS Phytoplasma diseases of medicinal and aromatic plants occur worldwide; however, the majority of the reports are There are several studies over the last decade in which from Europe and southeastern Asian countries (Table 1). the effects of phytoplasma presence on phytochemical con- Many of these diseases either were previously of unknown tent and other secondary metabolites were investigated in etiologies or mistakenly presumed to be induced by virus. symptomatic plants using mainly chromatographic, spec- Phytoplasma diseases of medicinal and aromatic plants trometric and molecular based-methods. affect plant species belonging to over 70 families, most- ly to Apiaceae and Asteraceae. They differ considerably St. John’s wort. The paper by Bruni et al. (2005) showed in geographic distribution and size of the various taxo- that qualitative and quantitative phytochemical changes nomic groups and subgroups of the associated phytoplas- occurred in Hypericum perforatum (St. John’s wort) ‘Zorzi’ mas. It appears that subgroup 16SrI-B phytoplasmas are plants infected with a 16SrVII phytoplasma (‘Candidatus Journal of Plant Pathology (2016), 98 (3), 379-404 Marcone et al. 381

Phytoplasma fraxini’) and showing yellows and witches’ the therapeutic effects of essential oils extracted from M. broom symptoms, in comparisons to healthy plants. The fistulosa plants doubly infected with the above mentioned total flavonoid and naphthodianthrone contents of dis- phytoplasmas. eased plants were lower than those of healthy ones (12.55 versus 6.74 mg/g and 1.41 versus 2.29 mg/g, respectively). Hyssop. Essential oils from Hyssopus officinalis (hys- Among flavonoid and naphthodianthrone components, sop) plants affected by the hyssop yellows disease, which is affected plants showed markedly decreased levels of ru- mostly associated with a 16SrXII-A phytoplasma, showed tin (1.96 versus 4.96 mg/g), hyperoside (2.38 versus 3.04 lower contents of isopinocanfone and trans-pinocanfone mg/g), isoquercitrin (1.47 versus 3.50 mg/g), amentoflavone than those of healthy plants. These compounds occurred (0.12 versus 0.39 mg/g) and pseudohypericin (1.41 versus at a rate of 29 and 3.92%, respectively, in diseased plants, 2.29 mg/g), whereas the levels of hypericin, quercitrin, and whereas amounted to 44.7 and 6.2% respectively, in quercetin were not significantly reduced. In contrast, the healthy plants. Conversely, the limonene content of es- amount of chlorogenic acid, a phenylpropane component, sential oils from diseased H. officinalis plants was 8.87% was higher in diseased plants that in healthy ones (1.56 ver- whereas that from healthy plants was 1.86% (Bellardi and sus 0.77 mg/g). Moreover the yield of volatile fraction, i.e., Bertaccini, 2005; Bertaccini et al., 2005). essential oils, was drastically reduced in diseased plants (0.11 versus 0.75% in healthy plants) and these oils showed Purple coneflower. In Echinacea purpurea (purple cone- an increase in sesquiterpenes (β-caryophyllene, β-copaene, flower) plants infected with a subgroup 16SrIX-C phyto- γ-amorphene, δ-elemene, α-humulene, and germacrene D), plasma and showing symptoms of phyllody and foliar red- from 63.52 to 75.01%, and a significant decrease of mono- dening the contents of cichoric acid and main caffeic acid terpene hydrocarbons (from 8.63 to 4.14%) and aliphatic derivatives were lower than those of healthy plants (15.38 compounds (from 6.31 to 2.58%). Flavonoids, naphthodi- versus 18.35 mg/g and 18.15 versus 20.82 mg/g, respec- anthrones and essential oils are major phytochemicals of tively). No significant differences between diseased and the H. perforatum drugs, which provide medical and/or healthy plants were found in alkamide contents (Pellati human health benefits. et al., 2011). Diseased purple coneflower plants showed a yield of essential oils, which differed slightly from that of Gum weed. Grindelia robusta (gum weed) plants in- healthy plants (0.026 versus 0.029% in healthy plants). Sig- fected by the aster yellows agent ‘Ca. P. asteris’, subgroup nificant differences between diseased and healthy plants 16SrI-B, contained less essential oils than healthy plants in the components of essential oils were observed for (0.11 versus 0.14%) (Bertaccini et al., 2008, 2011; Bellardi limonene (4.4 versus 2.2% in healthy plants), cis-verbenol et al., 2009). Forty-two compounds were identified in the (5.7 versus 1.8% in healthy plants), verbenone (11.6 ver- essential oils of both healthy and diseased plants. The sus 2.7% in healthy plants), carvone (2.5 versus 0.8% in levels of most of these compounds were lower in essen- healthy plants), germacrene D (8.5 versus 10.8% in healthy tial oils of diseased plants than in those of healthy plants. plants), caryophyllene oxide (3.3 versus 4.5% in healthy However, levels of monoterpenes such as limonene (9.34 plants), and spathulenol (3.2 versus 4.4% in healthy plants) versus 4.21%), borneol (21.34 versus 15.02) e bornyl acetate (Pellati et al., 2011). (8.91 versus 4.44%) were higher in infected plants than in healthy ones. Pellitory. Flavonoid contents of Parietaria officinalis and P. judaica (pellitory) plants were severely affected by Wild bergamot. Essential oils extracted from Mo- 16SrXII-A phytoplasmas. Kaempeferol and isorhamne- narda fistulosa (wild bergamot) plants showing symp- tin compounds could not be detected in diseased plants, toms of virescence, yellowing and stunting, which were while they occurred at concentrations of 47.56 and 22.28 doubly infected with subgroup 16SrI-B and 16SrXII- mg/100 g of dry weight, respectively, in healthy plants. Al- A phytoplasmas, presented an increase in the amount so, quercetin content was lower in diseased plants than in of some monoterpenes such as α-thujene, α- and healthy ones (10.26 versus 59.43 mg/100g of of dry weight) β-pinene, and β-phellandrene as well as in the amount of (Bellardi et al., 2008). α-caryophyllene and a marked decrease in the amount of thymol, compared to healthy plants. However, essential Pyrethrum. Tanacetum cinerariifoliumm (pyrethrum) is oils extracted from symptomless M. fistulosa plants, which a valuable source of the secondary metabolite pyrethrin, were infected by 16SrXII-A phytoplasma alone, showed widely used for environmentally friendly insecticides. In only a significant increase in the thymol content and a vitro-grown plants of pyrethrum, experimentally infected marked decrease in the amount of monoterpenes, com- with a subgroup 16SrIII-B phytoplasma, showed a marked pared to healthy plants (Contaldo et al., 2011). Thymol decrease of pyrethrin I and pyrethrin II contents, com- is a major compound of plants having antibacterial and pared to healthy in vitro-grown plants. The decrease was antimycotic properties such as M. fistulosa. Therefore, less pronounced in plants grown on Murashige and Skoog further sudies are needed to verify the maintainance of (MS) medium than in those on MS medium supplemented 382 Phytoplasma diseases Journal of Plant Pathology (2016), 98 (3), 379-404 with 3 µM IAA and 2 µM BAP (Ambrožič-Dolinšek et In particular, it has been shown that as a consequence al., 2008). of the infection of periwinkle plants with clover phyllody phytoplasma, (16SrIII-B subgroup), the content of terpe- Spanish broom. The paper by Mancini et al. (2010a) has noid indole alkaloids such as vindoline, ajmalicine, ser- shown that the yield of essential oils extracted from flow- pentine, vinblastine and vincristine increased. The total ers of Spartium junceum (Spanish broom) plants affected alkaloid content of dry weight was 550.96 μg/g, whereas by the spartium witches’ broom (SpaWB) disease was a that of healthy plants was 452.48 μg/g (Favali et al., 2004). little bit lower than that of healthy plants (0.004 versus However, the level reached by each compound in diseased 0.015%). Also, essential oils from healthy and diseased plants greatly differed among the plant organs. Vinblastine plants were qualitatively different. Substantial amounts of reached its highest concentration in the roots of infect- sesquiterpenes and a marked decrease in the amount of ed plants (148.44 μg/g), whereas it was not detectable or n-alkanes and aliphatic compounds occurred in the es- present at very low level (< 0.05 μg/g) in those of healthy sential oils from flowers of diseased plants. Sesquiterpenes plants. The content of vindoline (precursor of vinblas- were detected only in the essential oils of diseased plants. tine) increased in diseased leaves (222.00 versus 131.90 Approximately one third of the essential oils of infected μg/g of healthy plants) and stems (13.22 versus < 0.05 μg/g plants was represented by six sesquiterpenes (30.5%). of healthy plants) but decreased in diseased roots (< 0.05 Among them, five (25.5%) were oxygenated compounds versus 142.95 μg/g of healthy plants). Also, phytoplasma with τ-cadinol (19.2%) as the main component. In both infections led to a significant, two- to four-fold increase healthy and diseased plants, the main constituents were in chlorogenic acid in periwinkle, compared to healthy n-alkanes, which occurred at rate of 55.2 and 38.8%, plants (Choi et al., 2004). Work by Srivastava et al. (2014) respectively: tricosane (14.4%), pentacosane (7.3%) and has shown that in flowers of periwinkle plants infected heptacosane (4.6%) were the main components in healthy with a 16SrI-B phytoplasma the contents of vindoline, plants, whereas tricosane (5.5%), nonacosane (5.3%) and catharanthine, and vincristine plus vinblastine were two-, triacontane (5.0%) were prevalent in diseased plants. Ali- ten-, and four-fold higher, respectively, than those of phatic compounds occurred at a rate of 4.5% in diseased healthy flowers, whereas the contents of serpentine plus plants, whereas they amounted to 18.7% in healthy plants ajmalicine were lower than those of healthy flowers. How- (Mancini et al., 2010a). Great differences also occurred ever, in the leaves there were no significant differences in the content of alkaloid compounds between healthy between healthy and infected plants. Also, several genes and diseased Spanish broom plants: its content was con- including some involved in mevalonate pathway of the ter- siderably higher in samples of infected plants. Seven dif- penoid indole alkaloid biosynthesis system, namely geranyl ferent alkaloids were identified only in diseased plants. geranyl pyrophosphate synthase, geraniol 10 hydroxylase, These compounds included N-methylcytisine, its isomer, desacetoxyvindoline-4-hydroxylase, strictosidine synthase, N-formylcytisine and a hydroxy-substituted derivative of secologanin synthase, and deacetylvindoline-4-O-acetyl- sparteine. Four alkaloids including hydroxy-derivatives of transferase were expressed at higher levels in flowers of cytisine and anagyrine were shared by both healthy and diseased periwinkles than in those of healthy plants (Sriv- diseased plants. All identified alkaloids were of the qui- astava et al., 2014). Over the last few years, many attempts nolizidine type (Mancini et al., 2010b). have been made to boost the yield of terpenoid indole al- kaloids in periwinkle. Despite the progress made, they still Periwinkle. Catharanthus roseus (periwinkle) is a me- cannot be successfully produced on an industrial scale, dicinal plant of pharmaceutical interest for its capacity owing to several biological and technological constraints. to biosynthesize more than 130 alkaloids, most of which The various means by which terpenoid indole alkaloid ac- have pharmacological activities. Among these, there are cumulation can be increased include biotic elicitors such terpenoid indole alkaloids, including vinblastine and vin- as phytoplasmas (Zhou et al., 2009). Therefore, phytoplas- cristine, which are used for their antineoplastic activity ma infections in periwinkle, in spite of the detrimental in the treatment of many cancers, and ajmalicine and ser- effects on plant host, could be considered as beneficial pentine, which are used as antihypertensive and sedative, from the pharmaceutical point of view. respectively (Zhou et al., 2009; Pan et al., 2016). However, terpenoid indole alkaloids are produced in periwinkle only Grapevine. Grapevine yellows (GY) are diseases of Vi- in very small amounts and usually have some chiral cen- tis vinifera (grapevine) characterized by similar symptoms tres. They are therefore difficult to synthesize chemically, but differing in associated phytoplasmas and epidemiol- making expensive their large scale production (Zhou et ogy. Infections of grapevine plants by the “stolbur” agent al., 2009). Phytoplasma infections in periwinkle cause an ‘Ca. P. solani’, subgroup 16SrXII-A, during the early stages increase of metabolites related to the biosynthetic path- of shoot lignification induced a significant accumulation ways of terpenoid indole alkaloids (loganic acid, secolo- of several phenolic compounds including hydroxycinnamic ganic, vindoline) and phenylpropanoids (chlorogenic acid acid, monolignol derivatives, flavanone, ellagic acid de- and polyphenols) (Choi et al., 2004; Favali et al., 2004). rivatives, flavonols, flavanols and stilbenoids (Rusjan and Journal of Plant Pathology (2016), 98 (3), 379-404 Marcone et al. 383

Mikulic-Petkovsek, 2015). The significantly higher con- Proteomic studies also revealed that a number of proteins centration of hydroxycinnamic acid, monolignol deriva- were differentially expressed in grapevine cv Nebbiolo tives and flavanone in shoots of diseased plants, compared plants infected by the “flavescence dorée” phytoplasma, a to healthy ones, is a clear evidence that phenylpropanoid member of the 16SrV group, compared to healthy plants. and cinnamate/monolignol pathways were altered after the Among the differentially expressed proteins, a chalcone phytoplasma infections, thereby leading to lack or incom- isomerase was strongly up-regulated in affected plants plete shoot lignification (Rusjan and Mikulic-Petkovsek, (Margaria and Palmano, 2011; Margaria et al., 2013). 2015). ‘Ca. P. solani’ infections also induced an accumu- lation, mainly during the early phenological stages, in the leaves of diseased grapevine plants, of total phenols, CONCLUSIONS AND OUTLOOK hydroxycinnamic acid, flavonols and flavanols. Further- more, infected leaves showed a marked activity increase This review is the first to compile a comprehensive list of phenylalanine ammonia liase (PAL), chalcone synthase of phytoplasmas and phytoplasma diseases affecting me- (CHS), chalcone isomerase (CHI), flavanone 3-hydroxylase dicinal and aromatic plants as reported in the last years. (FHT) and polyphenoloxidase (PPO), and a decrease of Newly discovered diseases of such kind of plants are in- peroxidase (POD), compared to healthy plants, through- creasingly being attributed to phytoplasma presence. This out the whole growing season. In addition, chlorophyll and rapid increase may be related to the fact that the use of carotenoid contents were considerably reduced in infected chemical insecticides to control insect vectors of phyto- leaves (Bertamini et al., 2002; Landi and Romanazzi, 2011; plasmas is not allowed on medicinal and aromatic plants, Endeshaw et al., 2012; Rusjan et al., 2012a). Investigations whereas insect control and/or management by other, on the accumulation of phenolic compounds in berries environmentally-friendly means is not fully satisfactory. of “stolbur”-affected grapevine plants, at three different Phytoplasma diseases of medicinal and aromatic plants phenological stages such as veraison, berry softening and severely reduce yield and quality of crops and longevity berries ripe for harvest, showed that the total phenolic of plants. Changes in the composition of secondary me- content of berries from diseased plants was higher than tabolites occurring in diseased plants are related to the that of berries from healthy plants at veraison and berry role of phytoplasmas in triggering plant defense responses softening, whereas the opposite was true at stage of berries in which, however, the levels of valuable phytochemicals ripe for harvest (Rusjan et al., 2012b). Hydroxycinnamic are greatly affected. An exception is represented by peri- acids and flavanols content was higher in berries from winkle in which an accumulation of pharmaceutically diseased plants, compared to healthy ones only at berry important compounds such as vinblastine and vincristine softening stage, whereas the content of flavonols in ber- occurs upon phytoplasma infection. Also, because the ries from diseased plants proved to be considerably lower beneficial properties of medicinal and aromatic plants than that of healthy plants in each of the three pheno- can be related to combinations of phytochemicals act- logical stages (Rusjan et al., 2012b). Decreased contents of ing collectively or synergistically, the alteration of a single phenolic compounds especially flavonols in berries ripe phytochemical component could potentially affect the ef- for harvest greatly impair quality of grape and wine and ficacy of the plant material (Briskin, 2000). Therefore, any their antioxidant properties (Rusjan et al., 2012b). Grape variation of the chemical composition of medicinal and berries are valuable nutraceuticals mainly due to the pres- aromatic plants would need to be investigated by phar- ence of different types of flavonoids such as flavonols and macological studies aimed at evaluating the plant mate- anthocyanins and are widely used in pharmaceutical and rial effectiveness. The impact of phytoplasma infections cosmetic industries (Rusjan et al., 2008). Several genes on medicinal and aromatic plants should be taken into involved in secondary metabolism were differentially ex- account in promoting good agricultural pratices for culti- pressed in grapevine plants upon ‘Ca. P. solani’ infection. vation and propagation of these plants and for the develop- Among these, PAL, CHS, FHT, dihydroflavonol 4-reduc- ment of effective and standardised phytopharmaceutical tase, leucoanthocyanidin dioxygenase, flavonol synthase, and nutraceutical products. Moreover, further studies are beta-carotene hydroxylase and carotenoid cleavage di- needed to acquire knowledge on several other aspects of oxygenase 1 were significantly up-regulated in diseased the above mentioned diseases including disease manage- plants, compared with healthy ones (Albertazzi et al., 2009; ment, phytoplasma-insect vector relationships and role of Hren et al., 2009a; Landi and Romanazzi, 2011). Genes phytoplasmas in eliciting secondary metabolites which can encoding Myb transcription factors were down-regulated be pharmaceutically important. in highly susceptible grapevine cv Chardonnay plants by ‘Ca. P. solani’ infections. Since Myb transcription factors are essential for lignin biosynthesis, down-regulation of these genes may be another factor accounting for the lack of, or incomplete, shoot lignification in diseased grape- vine plants (Albertazzi et al., 2009; Hren et al., 2009a). 384 Phytoplasma diseases Journal of Plant Pathology (2016), 98 (3), 379-404

Table 1. Phytoplasma diseases of medicinal and aromatic plants.

Family Common Disease Phytoplasma(s) Geographic Reference Genus/species name associateda distribution

Acanthaceae Andrographis paniculata Kalmegh Kalmegh witches’ 16SrII-D India Saeed et al., 2015 broom Agavaceae Agave tequilana Blue agave Agave lethal 16SrIV Mexico González-Pacheco et al., 2014 yellowing Amaranthaceae Achyranthes aspera Prickly chaff flower Achyranthes yellows 16SrI India Raj et al., 2009a Amaranthus retroflexus Common amaranth Unnamed 16SrV-B, 16SrXII-A China, Czech Republic, Fialová et al., 2009; Yang et al., 2011; Mori Italy et al., 2015 Amaranthus Grain amaranth Unnamed 16SrII, 16SrIII Mexico Rojas-Martinez et al., 2009; Ochoa- hypochondriacus Sanchez et al., 2009; Pérez-López et al., 2016 Amaranthus cruentus Grain amaranth Unnamed 16SrII Mexico Ochoa-Sanchez et al., 2009 Amaranthus spp. Amaranth Amaranth yellows 16SrI-B, 16SrII, 16SrXII-A USA, India, Turkey Borth et al., 2006; Arocha et al., 2009; Özdemir et al., 2009 Chenopodium album Lambsquarters Chenopodium 16SrII, 16SrIII, 16SrXII-A Europe, Turkey Tolu et al., 2006; Özdemir et al., 2009; yellows Safarova et al., 2011; Mori et al., 2015 Anacardiaceae Pistacia palaestina Terebinth Unnamed 16SrIX-C Lebanon Casati et al., 2016 Apiaceae Amni majus Queen Anne’s lace Queen Anne’s lace 16SrI-B Canada Wang and Hiruki, 2005 yellows Anethum graveolens Dill Dill yellows 16SrI-A, -B, -C, 16SrV-A, USA, Italy Boccardo et al., 2002; Lee et al., 2003, 16SrXII-A 2004 Anthriscus cerefolium Curled chervil Anthriscus reddening N.D. Canada Hwang et al., 1998 Apium graveolens Celery Celery yellows 16SrI-A, -B, 16SrII-E, Europe, North America, Seemüller et al., 1998; Tran-Nguyen et al. 16SrIII; 16SrXII-A, -B Japan, Australia, New 2003; Lee et al., 2004; Carraro et al., 2008; Zealand Fialová et al., 2009; Wang and Hiruki, 2005; Ivanovi et al., 2011; Liefting et al., 2011; Maejima et al., 2014 Apium graveolens Celery Celery stunting and 16SrI-C Czech Republic Fránová and Špak,ć 2013 phyllody Bupleurum falcatum Chai hu Chai hu yellows 16SrI-A Canada Chang et al., 2004 Carum carvi Caraway Caraway yellows N.D. Canada Hwang et al., 1997a Carum carvi Caraway Caraway yellows 16SrXII-A Serbia Pavlovi et al., 2014a Coriandrum sativum Coriander Coriander yellows 16SrI-A, -B USA Lee et al., 2004 Daucus carota Carrot Carrot yellows 16SrI-A, -B, 16SrIX, North America, Europe, Chang etć al., 2004; Lee et al., 2004; 16SrXII-A Japan Maejima et al., 2014; Marchi et al., 2015 Eryngium alpinum Queen of the Alps Eryngium yellows 16SrI-M Lithuania Samuitiene et al., 2006, 2007 Foeniculum vulgare Fennel Fennel phyllody 16SrII India Bhat et al., 2008 Levisticum officinale Lovage Levisticum yellows 16SrXII-A Serbia Pavlovi et al., 2014a Petroselinum spp. Parsley Parsley yellows 16SrI-A, -B, 16SrXII-A Canada, Serbia Khadhair et al., 1998; Lee et al, 2003, 2004; Wangć and Hiruki, 2005; Mitrovi et al., 2013 Pimpinella anisum Anise Unnamed 16SrI Canada Olivier et al., 2009 ć Trachyspermum ammi Ajwain Ajwain yellows 16SrVI India Samad et al., 2011a Apocynaceae Catharanthus roseus Periwinkle Mexican periwinkle 16SrXIII-A (‘Ca. P. Mexico Davis et al., 2016 virescence hyspanicum) Catharanthus roseus Periwinkle Malaysian periwinkle 16SrXXXII-A (‘Ca. P. Asia Nejat et al., 2013 virescence malaysianum’) Catharanthus roseus Periwinkle Periwinkle yellows 16SrI, 16SrII, 16SrIII, Europe, Americas, Asia Seemüller et al., 1998; Lee et al., 2000, and phyllody 16SrVI, 16SrIX, 16SrXII 2004, 2012; Torres et al., 2004; Ayman et al., 2010; Chen et al., 2011; Galdeano et al., 2013; Mitrovi et al., 2013; Caicedo et al., 2015; Khanna et al., 2015; Pérez-López et al., 2016 ć Periploca aphylla Milk broom Periploca aphylla 16SrXXX (‘Ca. P. Iran Faghihi et al., 2010 witches’ broom tamaricis’)-related Calotropis gigantea Crown flower Calotropis yellows 16SrVI India Priya et al., 2010 Tylophora asthmatica Indian ipecac Tylophora asthmatica 16SrII-D India Madhupriya et al., 2014 little leaf Arecaceae Roystonea regia Royal palm Royal palm yellow 16SrI Malaysia Naderali et al., 2015 decline Asclepiadaceae Asclepias fruticosa (syn. Swan plant Swan plant yellows 16SrXII-B New Zealand Liefting et al., 2011 Gomphocarpus fruticosa) Journal of Plant Pathology (2016), 98 (3), 379-404 Marcone et al. 385

Table 1 (continued). Phytoplasma diseases of medicinal and aromatic plants.

Asclepias physocarpa Balloonplant Balloonplant yellows 16SrI-B, 16SrXII-A Italy, Iran d’Aquilio et al., 2002; Bellardi and (syn. Gomphocarpus Bertaccini, 2005; Bertaccini et al., 2006; physocarpus) Babaie et al., 2007 Asclepias syriaca Milkweed Milkweed yellows 16SrIII-F North America Lee et al., 2000 Asparagaceae Asparagus officinalis Asparagus Asparagus stem 16SrI-B Czech Republic Fránová and Petrzik, 2010 fasciation Asparagus officinalis Asparagus Asparagus yellows 16SrI-A Canada Wang and Hiruki, 2005 Asteraceae Arnica montana Mountain arnica Arnica virescence 16SrIII-B Serbia Pavlovic et al., 2012a Artemisia scoparia Redstem Artemisia scoparia 16SrXII-A China Yu et al., 2016 wormwood witches’ broom Artemisia vulgaris Mugwort Artemisia yellows 16SrXII-A Italy Mori et al., 2015 Bellis perennis Daisy Daisy yellows 16SrI-A, 16SrIII-J Lithuania, Argentina Samuitiene et al., 2007; Galdeano et al., 2013 Calendula officinalis Pot marigold Calendula virescence 16SrI-B, 16SrII, 16SrXII-A Italy, Serbia, Canada, Hwang et al., 1977b; Marcone et al., and phyllody Iran 2000; Lee et al., 2004; Wang and Hiruki, 2005; Esmailzadeh-Hosseini et al., 2011; Pavlovic et al., 2014b Calendula arvensis Field marigold Unnamed 16SrII-E Italy Tolu et al., 2006 Centaurea solstitialis Yellow starthistle Centaurea solstitialis 16SrVI Italy Faggioli et al., 2004 virescence Cichorium intybus Common chicory Chicory phyllody 16SrII-E, 16SrIX, Italy, Serbia, Australia Tran-Nguyen et al. 2003; Marcone, 2011; 16SrXII-A Ermacora et al., 2013; Pavlovic et al., 2014c Cirsium arvense Creeping thistle Cirsium yellows and 16SrXI-E (‘Ca. P. cirsii’) Czech Republic Šafá ová et al., 2016 stunting Cirsium arvense Creeping thistle Cirsium yellows 16SrI-M., 16SrIII, 16SrIX, Europe Seemüllerř et al., 1998; Jomantiene et al., 16SrXII-A 2000, 2002; Lee et al., 2004; Bellardi and Bertaccini, 2005; Fialová et al., 2009; Marchi et al., 2015 Cirsium arvense Creeping thistle Cirsium multiple 16SrIII-B Serbia Ran i et al., 2005; Jakovljevi et al., 2015 inflorescence Cynara scolymus Artichoke Artichoke 16SrXII Spain Battleč ć et al., 2007 ć degeneration Dittrichia viscosa (syn. False yellowhead Unnamed 16SrIX-C Lebanon Casati et al., 2016 Inula viscosa) Echinacea angustifolia Narrow-leaved Purple coneflower 16SrXII-A Serbia Pavlovi et al., 2014a purple coneflower yellows Echinacea purpurea Purple coneflower Purple coneflower 16SrI-A, -B, -C; 16SrIII-B; North America, Europe Khadhairć et al., 1997; Hwang et al., 1977c; yellows 16SrIX-C; 16SrXII-A Lee et al., 2004, 2008; Wang and Hiruki, 2005; Bertaccini et al., 2009; Radisek et al., 2009; Fránová et al., 2009, 2013; Pavlovi et al., 2011; Pellati et al., 2011 Echinacea purpurea Purple coneflower Purple coneflower 16SrII-A Taiwan Tseng et al., 2012 witches’ broom ć Echinacea pallida Pale purple Pale purple 16SrII-D Australia Pearce et al., 2011 coneflower coneflower witches’ broom Echinops spinosissimus Hink Echinops witches’ 16SrIX Oman Al-Subhi et al., 2007 broom Grindelia robusta Gum weed Unnamed 16SrI-B Italy Bertaccini et al., 2008, 2011; Bellardi et al., 2009 Guizotia abyssinica Niger seed Niger seed phyllody 16SrI, 16SrII Iran, Australia Seemüller et al., 1998; Vaali et al., 2011 Ixeridium chinense China ixeris China ixeris 16SrI-C China Li et al., 2013 fasciation Lactuca serriola Prickly lettuce Prickly lettuce 16SrI-B, 16SrIX-C Iran, Lebanon Babaie et al., 2007; Salehi et al., 2007; yellows Sichani et al., 2014; Casati et al., 2016 Leucanthemum vulgare Oxeye daisy Oxeye daisy phyllody 16SrIII-B Italy Firrao et al., 1996 (syn. Chrysanthemum vulgare) Matricaria chamomilla Chamomile Chamomile witches’ 16SrXII-A Serbia Pavlovi et al., 2014a (syn. Chamomilla recutita) broom Parthenium hysterophorus Whitetop weed Parthenium witches’ 16SrI, 16SrII Asia Raj et alć., 2008a; Li et al., 2011a; Ahmad broom et al., 2015 Sonchus asper Grespino thorny Grespino thorny 16SrI-A USA Lee et al., 2004 yellows Sonchus spp. Sowthistle Unnamed 16SrI, 16SrIX, 16SrXII-A Europe, North America Borth et al., 2006; Khadhair et al., 2008; Marchi et al., 2015; Mori et al., 2015 Stevia rebaudiana Honey leaf plant Stevia decline 16SrXXIV-A India Samad et al., 2011b Tagetes erecta Marigold Marigold phyllody 16SrI-B, 16SrXII-A Americas, Europe, Asia, Loi et al., 1998; Rojas-Martínez et al., Turkey 2003; Raj et al., 2011a; Alp et al., 2016 Tagetes patula French marigold Marigold yellows 16SrI-A, -B Americas, Europe, Asia Bellardi and Bertaccini, 2005; Wang and Hiruki, 2005; Babaie et al., 2007; Sichani et al., 2014 386 Phytoplasma diseases Journal of Plant Pathology (2016), 98 (3), 379-404

Table 1 (continued). Phytoplasma diseases of medicinal and aromatic plants.

Tanacetum Pyrethrum Pyrethrum yellows 16SrI-A Canada Wang and Hiruki, 2005 cinerariifoliumm Tanacetum parthenium Feverfew Feverfew yellows 16SrI-B Canada, Iran Wang and Hiruki, 2005; Babaie et al., 2007 Taraxacum officinale Dandelion Dandelion yellows 16SrI, 16SrII-E, 16SrIII, Europe, Americas Seemüller et al., 1998; Jomantiene et al., 16SrIX, 16SrXII-A 2002; Lee et al., 2004; Wang and Hiruki, 2005; Hodgetts et al., 2009; Marcone, 2011; Mori et al., 2015 Tussilago farfara Coltsfoot Tussilago reddening 16SrXII-A Italy Romanazzi et al., 2009; Marchi et al., 2015 Balsaminaceae Impatiens balsamina Rose balsam Rose balsam phyllody 16SrI-D China Chang et al., 2011; Li et al., 2011b and virescence Berberidaceae Berberis thunbergii Red barberry Berberis phyllody 16SrV-B China Li et al., 2010a atropurpurea Betulaceae Alnus glutinosa Black alder Alder yellows 16SrV-C Europe Marcone, 2015 Bignoniaceae Tabebuia heterophylla Tabebuia Tabebuia witches’ 16SrIX Puerto Rico Caicedo et al., 2015 broom Brassicaceae Brassica spp. Brassicas Brassica phyllody and 16SrI, 16SrIII, 16SrIX, Europe, Americas, Asia Marcone et al., 2000; Lee et al., 2004, virescence 16SrXII-A 2012; Salehi et al., 2011; Trkulja et al., 2011; Mou et al., 2012; Rappussi et al., 2012; Eckstein et al., 2013 Eruca sativa Salad rocket Eruca sativa phyllody 16SrI-B Iran Esmailzadeh Hosseini et al., 2015a Raphanus raphanistrum Wild radish Wild radish yellows 16SrI-B Italy Marcone et al., 2000; Lee et al., 2004 Cannabaceae Cannabis sativa Hemp Hemp witches’ 16SrI, 16SrXIV-A India, Iran Raj et al., 2008b; Sichani et al., 2014; broom Chaube et al., 2015a Convolvulaceae Calystegia sepium Hedge bindweed Bindweed yellows 16SrXII-A Europe Langer and Maixner, 2004; Fialová et al., 2009; Coccinia grandis Ivy gourd Ivy gourd yellows 16SrXIV Thailand Sunpapao, 2014 Convolvulus arvensis Field bindweed Bindweed yellows 16SrX, 16SrI, 16SrXII-A, Europe, Israel Marcone et al., 1997a; Seemüller et al., 16SrII, 16SrIX 1998; Langer and Maixner, 2004; Bellardi and Bertaccini, 2005; Fialová et al., 2009; Murolo et al., 2010; Dafny Yelin et al., 2015; Marchi et al., 2015; Mori et al., 2015 Convolvulus arvensis Field bindweed Bindweed yellows 16SrXII-H (‘Ca. P. Italy, Serbia, Bosnia and Martini et al., 2012 convolvuli’) Herzegovina, Germany Caprifoliaceae Sambucus nigra Black elder Sambucus decline 16SrXII-A, -E Italy, Germany Lederer and Seemüller, 1991; Filippin et al., 2008 Sambucus racemosa European red elder Sambucus decline N.D. Germany Lederer and Seemüller, 1991 Caryophyllaceae Saponaria officinalis Common soapwort Saponaria yellows 16SrI-M, 16SrXII-A Serbia, Lithuania Lee et al., 2004; Josic et al., 2013 Silene orientalis Campion Silene virescence 16SrI-B, 16SrXII-A Lithuania Samuitiene et al., 2006, 2007; Berger et al., 2009 Cornaceae Cornus sanguinea Common dogwood Common dogwood 16SrXII-A, -E Italy, France Jarausch et al., 2001; Filippin et al., 2008 yellows Crassulaceae Rhodiola rosea Golden root Rhodiola yellows 16SrI-B Canada Hwang et al., 2009 Cucurbitaceae Momordica charantia Bitter gourd Bitter gourd little leaf 16SrI-B, 16SrII Myanmar, Indonesia, Sdoodee et al., 1999; Davis et al., 2003; and phyllody Thailand Win et al., 2014 Lagenaria siceraria Bottle gourd Lagenaria yellows 16SrIII-Y Brazil Montano et al., 2015a Sicana odorifera Sikana Unnamed 16SrIII Brazil Montano et al., 2007 Cupressaceae Juniperus occidentalis Western juniper Juniper witches’- 16SrIX-F USA (Oregon) Davis et al., 2010 broom Elaeagnaceae Elaeagnus angustifolia Russian olive Russian olive witches’ 16SrI Iran Rashidi et al., 2010 broom Ericaceae Vaccinium corymbosum Highbush Blueberry stunt 16SrI-E, 16SrXII-A Canada, Serbia Pavlovi et al., 2014a; Arocha Rosete et blueberry al., 2015 ć Journal of Plant Pathology (2016), 98 (3), 379-404 Marcone et al. 387

Table 1 (continued). Phytoplasma diseases of medicinal and aromatic plants.

Vaccinium macrocarpon American Cranberry false- 16SrIII-Y USA Lee et al., 2014 cranberry blossom Vaccinium myrtillus Blueberry Blueberry stunt and 16SrI-E, 16SrIII, 16SrIX-E USA, Europe Seemüller et al., 1998; Valiunas et al., witches’ broom 2004; Lee et al., 2012; Bagadia et al., 2013 Euphorbiaceae Acalypha indica Indian nettle Acalypha witches’ N.D. India Singh and Gupta, 2011; Singh et al., broom 2013a; Singh and Upadhyaya, 2015 Mallotus japonicus Food wrapper plant Mallotus witches’ 16SrI-B Korea Han et al., 2014 broom Mercurialis annua Annual mercury Annual mercury 16SrIII-B, 16SrXII-A Italy Bellardi and Bertaccini, 2005; Marchi et yellows al., 2015 Sapium sebiferum Chinese tallow tree Chinese tallow tree 16SrIII-Y China Gao et al., 2015a yellows Fabaceae Cassia italica Italian senna Cassia witches’ 16SrXXIX-A (‘Ca. P. Oman Khan et al., 2007a; Al-Saady et al., 2008 broom omanense’), 16SrIX Crotalaria pallida Smooth rattlepod Crotalaria little leaf 16SrII-D India Yadav et al., 2016 Dimorphandra spp. “Fava d’anta” tree Dimorphandra 16SrXIII Brazil Montano et al., 2015b witches’ broom Galega officinalis Galega Galega yellows 16SrIII-J, 16SrVII-A, Chile, Italy Bellardi and Bertaccini, 2005; Longone et 16SrX al., 2011; Zamorano et al., 2015 Medicago sativa Alfalfa Alfalfa witches’ 16SrI, 16SrII, 16SrIII-B, Europe, Americas, Asia, Seemüller et al., 1998; Peters et al., 1999; broom 16SrV-B, 16SrVI, Australia Khan et al., 2002; Pilkington et al., 16SrVII-C, 16SrXII-A 2003; Lee et al., 2004; Conci et al., 2005; Wang and Hiruki, 2005; Hodgetts et al., 2009; Li et al., 2012; Starovi et al., 2012; Esmailzadeh Hosseini et al., 2015b Mimosa pudica Sensitive plant Mimosa yellows 16SrI Indonesia Boa et al., 2010 ć Senna surattensis Sunshine tree Sunshine tree stem 16SrV, 16SrXII China Wu et al., 2012 fasciation Sophora alopecuroides Sophora root Sophora root yellows 16SrI, 16SrVI-D China, Iran Chen et al., 2013; Zibadoost and Rastgou, 2016 Sophora japonica Chinese scholar Sophora japonica 16SrV-B China Duduk et al., 2010; Yu et al., 2012; Ren et tree witches’ broom al., 2014 Spartium junceum Spanish broom Spartium witches’ 16SrX-D (‘Ca. P. spartii’), Italy, Spain Marcone et al., 1996a, 2004a; Torres et broom 16SrV-C al., 2002; Spallino et al., 2013; Contaldo et al., 2015 Tephrosia purpurea Wild indigo Tephrosia purpurea 16SrII-M India Yadav et al., 2014 witches’ broom Trigonella foenum greacum Fenugreek Fenugreek yellows 16SrXII-A Serbia Pavlovi et al., 2014a

Gentianaceae ć Centaurium erythraea Centaury Centaury virescence 16SrI-B Italy Paltrinieri et al., 2016 Enicostemma axillare Indian whitehead Enicostemma 16SrII-C India Abirami et al., 2012 witches’ broom Geraniaceae Geranium purpureum Little-robin Unnamed 16SrIX-C Lebanon Casati et al., 2016 Grossulariaceae Ribes rubrum Red currant Unnamed 16SrI-C Czech Republic P ibylová et al., 2011

Hypericaceae ř Hypericum perforatum St. John’s wort St. John’s wort 16SrVII, 16SrXII-A Italy, Serbia Paltrinieri et al., 2002; Bellardi and decline Bertaccini, 2005; Bruni et al., 2005; Pavlovi et al., 2012b Hypericum barbatum St. John’s wort St. John’s wort 16SrXII-A Serbia Pavlovi et al., 2012b decline ć ć Lamiaceae Hyssopus officinalis Hyssop Hyssop yellows 16SrXII-A, 16SrI Italy Bellardi and Bertaccini, 2005; Bertaccini et al., 2005 Lavandula spp. Lavender Lavandula yellows 16SrXII-A, 16SrI, 16SrVI Europe, Israel Seemüller et al., 1998; Marzachì et al., 1999; Langer and Maixner, 2004; Weintraub et al., 2007; Gaudin et al., 2011 Melissa officinalis Lemon balm Melissa yellows 16SrXII-A Serbia Pavlovi et al., 2014a Mentha×piperita Peppermint Peppermint stunt 16SrXII-A Serbia Mitrovi et al., 2016 Monarda fistulosa Wild bergamot Monarda yellows 16SrI-B, 16SrII, 16SrXII-A Canada, Italy Khadhairć et al., 1997; Hwang et al., 1977d; Wang etć al., 1998; Wang and Hiruki, 2005; Bellardi et al., 2011; Contaldo et al., 2011 Ocimum basilicum Basil Basil little leaf 16SrI Cuba Arocha et al., 2006 Origanum vulgare Oregano Oregano reddening 16SrXII-A Serbia Pavlovi et al., 2014a Rosmarinus officinalis Rosemary Rosemary yellows 16SrXII-A, 16SrI-B Italy Contaldo et al., 2012 Salvia miltiorrhiza Red sage Salvia miltiorrhiza 16SrXII-A China Yang etć al., 2016a red leaf Salvia sclarea Clary sage Clary sage yellows 16SrX Italy Bellardi and Bertaccini, 2005 388 Phytoplasma diseases Journal of Plant Pathology (2016), 98 (3), 379-404

Table 1 (continued). Phytoplasma diseases of medicinal and aromatic plants.

Thymus vulgaris Thyme Unnamed 16SrXII-A Spain Battle et al., 2000 Lauraceae Cinnamomum cassia Chinese cinnamon Cinnamon yellow leaf 16SrII China Yang et al., 2016b Liliaceae Allium altyncolicum Unknown Unnamed 16SrI-B Czech Republic Navrátil et al., 2000 Allium ampeloprasum Leek Leek proliferation 16SrI-B, 16SrXII-A Czech Republic, Italy Bertaccini et al., 1999 Allium cepa Onion Onion yellows 16SrI-B, -A, -L, -M; 16SrVI Italy, Japan, USA, Marcone et al., 2000; Khadhair et al., Canada, Lithuania, 2002; Lee et al., 2003, 2004; Jomantiene Pakistan et al., 2010; Maejima et al., 2014; Ahmad et al., 2015 Allium fistulosum Welsh onion Onion yellows 16SrI-B Japan Maejima et al., 2014 Allium sativum Garlic Garlic decline 16SrIII-J Argentina, Canada Conci et al., 1998; Khadhair et al., 2002; Galdeano et al., 2013 Malvaceae Abelmoschus esculentus Okra Okra bunchy top 16SrI, 16SrV, 16SrXII Mauritius, India, Fahmeed et al., 2009; Gungoosingh- Pakistan Bunwaree et al., 2011; Kumar et al., 2012a Hibiscus rosa-sinensis Chinese hibiscus Hibiscus yellows and 16SrI India Chaturvedi et al., 2010 little leaf Hibiscus rosa-sinensis Chinese hibiscus Hibiscus witches’ 16SrXV-A (‘Ca. P. Brazil Montano et al., 2001, 2011a broom brasiliense’), 16SrXII Hibiscus sabdariffa Roselle Roselle phyllody 16SrI, 16SrV-D India, Taiwan Biswas et al., 2013a; Tseng et al., 2014 Malva sylvestris Mallow Mallow yellows 16SrI-B, 16SrV-E, Italy, France, Lebanon Seemüller et al., 1998; Jarausch et al., 16SrIX-C, 16SrXII-A 2001; Mori et al., 2015; Casati et al., 2016 Malvastrum False mallow Unnamed 16SrII South America Pérez-López et al., 2016 coromandelianum Sida cordifolia Flannel weed Sida little leaf 16SrII-C Australia, Mali Davis et al., 1997a; Marzachì et al., 2009 Meliaceae Melia azedarach Chinaberry Chinaberry yellows 16SrI-B, 16SrIII-J, Bolivia, Vietnam Harrison et al., 2003, 2006 16SrXIII-C Melia azedarach Chinaberry Chinaberry yellows 16SrIII-B, 16SrXIII-C (‘Ca. South America Galdeano et al., 2013; Pérez-López et al., P. meliae’) 2016; Fernández et al., 2016 Melia azedarach Chinaberry Melia witches’ broom 16SrI-B China, Korea Han et al., 2015 Toona ciliata Toon Toon yellows 16SrI-B India Ayman et al., 2010 Menispermaceae Tinospora cordifolia Heart-leaved Tinospora flat stem N.D. India Somashekhara Achar et al., 2015 moonseed Corchorus capsularis White jute White jute little leaf 16SrV India Biswas et al., 2013b Corchorus olitorius Jute Jute phyllody 16SrII-D Turkey Cagirgan et al., 2014; Özdemir and Cagirgan, 2015 Moraceae Brussonetia papyrifera Paper mulberry Paper mulberry 16Sr -B China Mei et al., 2016 yellows Streblus asper Toothbrush tree Streblus asper little 16SrIΙ India Maurya et al., 2014 leaf Myrtaceae Eucalyptus spp. Eucalypt Eucalyptus little leaf 16SrV, 16SrI-B, -C, 16SrII Italy, India, China, Marcone et al., 1996b, 1997b; Camele et Sudan, Iran, Brazil al., 1999; de Souza et al., 2015; Marcone, 2015; Salehi et al., 2016a Ugni molinae Murta Murta witches’ 16SrIII-J, 16SrV-A, Chile Arismendi et al., 2010, 2011a, 2011b broom 16SrVII-A Myrtus communis Myrtle Myrtle yellows 16SrI-B, 16SrII-F, Italy Camele et al., 1999; Garau et al., 2005; 16SrIII-B, 16SrV-A, Prota et al., 2007 16SrX-A, 16SrXII-A Nyctaginaceae Mirabilis jalapa Four o’clock flower Mirabilis little leaf 16SrII India, Israel Sobolev et al., 2007; Weintraub et al., 2007; Kumar et al., 2012b Oleaceae Jasminum sambac Arabian jasmine Arabian jasmine 16SrI, 16SrII, 16SrXI-B Italy, Oman, India Marzachì et al., 1999; Al-Zadjali et al., witches’ broom 2007; Madhupriya et al., 2015a Ligustrum ovalifolium California privet Ligustrum witches’ 16SrII Turkey Ça lar and Elbeaino, 2013 broom Olea europaea Olive Olive witches’ broom 16SrI-B, -C, 16SrIII, 16SrV, Italy, Spain, Iran Seemüllerğ et al., 1998; Font et al., 1998; 16SrXII-A Marzachì et al., 1999; Pasquini et al., 2000; Lee et al., 2004; Ahangaran et al., 2006; Ça layan et al., 2011

Onagraceae ğ Oenothera biennis Evening primrose Oenothera reddening 16SrXII-A, 16SrI-B Serbia, USA Hwang et al., 1998; Seemüller et al., 1998; and virescence Adamovic et al., 2014 Paeoniaceae Paeonia suffruticosa Tree peony Tree peony yellows 16SrXII China Gao et al., 2013 Journal of Plant Pathology (2016), 98 (3), 379-404 Marcone et al. 389

Table 1 (continued). Phytoplasma diseases of medicinal and aromatic plants.

Papaveraceae Escholtzia californica California poppy California poppy 16SrI-A Canada Wang and Hiruki, 2005 yellows Papaver rhoeas Corn poppy Papaver virescence 16SrI-B Italy Marcone et al., 2000 Pedaliaceae Pedalium murex Large caltrops Pedalium phyllody 16SrII-A India Babu et al., 2015 Sesamum indicum Sesame Sesame phyllody 16SrI-B, 16SrII-A, -C, -D, Asia, Turkey Khan et al., 2007b; Win et al., 2010; Catal 16SrIX et al., 2013; Ikten et al., 2014; Madhupriya et al., 2015b; Nabi et al., 2015, Singh et al., 2016 Phyllanthaceae Phyllanthus niruri Gale of the wind Phyllanthus little leaf 16SrI India Chaube et al., 2015b Piperaceae Piper nigrum Black pepper Black pepper 16SrI India Bhat et al., 2006 phyllody Piper nigrum Black pepper Coorg black pepper 16SrI-B India Adkar-Purushothama et al., 2009, 2011 yellows Plantaginaceae Plantago lanceolata English plantain Plantain yellows 16SrI-B, 16SrXII-A Czech Republic, Italy Fránová and Šimková, 2009; Marcone, 2011; Mori et al., 2015 Plantago major Broadleaf plantain Plantain yellows 16SrI-B, 16SrXII-A Germany, Italy, Serbia, Marcone et al., 2000; Lee et al., 2004; USA Bellardi and Bertaccini, 2005; Borth et al., 2006; Josic et al., 2012; Mori et al., 2015 Plantago coronopus Plantain Plantain virescence 16SrI-A Germany Marcone et al., 2000; Lee et al., 2004 Plumbaginaceae Limonium sinuatum Sea-lavender Limonium yellows 16SrI-A, -B, -C, -M Poland, Lithuania, Kami ska et al., 1999; Valiunas et al., Canada, Iran, Japan, 2001; Lee et al., 2004; Chung et al., 2005; Korea Samuitieneń et al., 2007; Babaie et al., 2007; Maejima et al., 2014 Limonium tataricum German statice Limonium yellows 16SrI Canada Chang et al., 2004 Limonium spp. Statice Limonium yellows 16SrI-B, 16SrII, 16SrV, Italy, Israel Gera et al., 2004; Abagnale et al., 2009; 16SrIX Paltrinieri et al., 2016 Poaceae Cymbopogon citratus Lemon grass Cymbopogon citratus 16SrII India Madhupriya et al., 2014 white leaf Cynodon dactylon Bermuda grass Bermuda grass white 16SrXIV-A, -C (‘Ca. P. Asia, Europe, Turkey, Marcone et al., 2004b; Arocha et al., 2005; leaf cynodontis’) Sudan, Australia, Cuba Rao et al., 2007; Salehi et al., 2009; Ça lar et al., 2013; Khanna et al., 2015; Mitrovi et al., 2015 ğ Cynodon dactylon Bermuda grass Bermuda grass white 16SrXII-A Serbia Mitrovi et al., 2012 ć leaf Digitaria sanguinalis Crab grass Digitaria white leaf 16SrXIV-A Italy, India Rao et alć., 2010; Marcone, 2011 Polygonaceae Polygonum aviculare Common knotgrass Polygonum yellows 6SrVII-A, 16SrXII-A Chile, Italy Berger et al., 2009; Longone et al., 2011 Portulacaceae Portulaca grandiflora Moss-rose purslane Portulaca little leaf 16SrVI India Ajayakumar et al., 2007; Samad et al., 2008 Portulaca oleracea Purslane Portulaca yellows 16SrI-B; 16SrXII-A Italy Marcone et al., 2000; Mori et al., 2015 Primulaceae Primula spp. Primrose Primula yellows and 16SrI-A, -B, -L Europe Lee et al., 2004; Fránová et al., 2016 virescence Punicaceae Punica granatum Pomegranate Pomegranate yellows 16SrI-A, 16SrXII-A Turkey Karimi et al, 2015; Gazel et al., 2016 Ranunculaceae Aconitum napellus Aconite Aconitum 16SrI-A, -L Lithuania Valiunas et al., 2001; Lee et al., 2004; proliferation Samuitiene et al., 2007 Rhamnaceae Hovenia dulcis Japanese raisin Japanese raisin 16SrV-B Asia Kamala-Kannan et al., 2011 witches’ broom Rhamnus catharticus Buckthorn Buckthorn witches’ 16SrXX-A (‘Ca. P. rhamni’) Europe Marcone et al., 2004a; Marcone, 2015 broom Rosaceae Crataegus monogyna Hawthorn Hawthorn yellows 16SrX-A, -C, -F Europe Tedeschi et al., 2009; Seemüller et al., 2011 Prunus spinosa Blackthorn European stone fruit 16SrX-F Europe Marcone et al., 2010, 2011 yellows Rosa alba Rose Rose little leaf 16SrI India Chaturvedi et al., 2009 Rosa damascena Damask rose Rose witches’ broom 16SrV-B-related India Saeed et al., 2016 Rosa multiflora Rose Rose dieback 16SrI-B Poland Kami ska et al., 2003

ń 390 Phytoplasma diseases Journal of Plant Pathology (2016), 98 (3), 379-404

Table 1 (continued). Phytoplasma diseases of medicinal and aromatic plants.

Rosa spp. Rose Rose yellows 16SrI, 16SrI-B, 16SrII, Iran, India, Italy, Jarausch et al., 2001; Kami ska et al., 16SrV-E, 16SrX-A, -C, -F France, Poland 2001; Kami ska and liwa, 2004; Bellardi and Bertaccini, 2005; Gao ńet al., 2008; Raj et al., 2011b;ń Aldaghi Śand Bertaccini, 2015 Rubus spp. Brambles Rubus stunt 16SrV-E (‘Ca. P. rubi’), Europe, Turkey, USA, Bertaccini et al., 1995a; Seemüller et al., 16SrI, 16SrIII, 16SrXII Pakistan, New Zealand 1998; Davies, 2000; Davis et al., 2001; Sertkaya et al., 2004; Borroto Fernández et al., 2007; Fahmeed et al., 2009; Reeder et al., 2010; Malembic-Maher et al., 2011; Cieslinska, 2011; Liefting et al., 2011 Spiraea salicifolia Bridewort Spiraea yellows 16SrV-B China Li et al., 2010b Spiraea spp. Spirea Spirea stunt 16SrIII-E USA Lee et al., 2000 Rubiaceae Coffea arabica Coffee Coffee crispiness 16SrIII Colombia Galvis et al., 2007 Coffea arabica Coffee Coffee witches’ 16SrIX Puerto Rico Caicedo et al., 2015 broom Ixora coccinea Ixora Ixora witches’ broom 16SrIX Puerto Rico Caicedo et al., 2015 Morinda citrifolia Bartondi Bartondi yellows N.D. India Sarwade et al., 2015 Rubia tinctorum Common madder Common madder 16SrVI-D Iran Zibadoost and Rastgou, 2016 little leaf Rutaceae Citrus paradisi Grapefruit Grapefruit yellows 16SrI, 16SrII-A-related China, Pakistan Fahmeed et al., 2009; Lou et al., 2014 Dictamus alba Dittany Dictamus albus 16SrI-B, 16SrIII-F Canada, Lithuania Wang and Hiruki, 2005; Valiunas et al., yellows 2007 Zanthoxylum schinifolium Prickly ash Prickly ash witches’ 16SrI Korea Han et al., 2013 broom Salicaceae Salix alba White willow Salix witches’ broom 16SrXII-A Serbia Pavlovi et al., 2014a Salix tetradenia Black mountain Salix witches’ broom 16SrI China Mou et al., 2014 willow ć Santalaceae Santalum album Sandal Sandal spike 16SrI-B India Lee et al., 2004; Khan et al., 2008 Sapindaceae Dimocarpus longan Longan Longan witches’ 16SrII, 16SrV, 16SrXII Vietnam Nguyen et al., 2012; Hoat et al., 2015 broom Melicoccus bijugatus Spanish lime Spanish lime 16SrIX Puerto Rico Caicedo et al., 2015 fasciation Sapotaceae Manilkara zapota Sapodilla Sapodilla witches’ 16SrII Cuba Acosta et al., 2009 broom Scrophulariaceae Digitalis lanata Woolly foxglove Foxglove yellows 16SrI-B Italy Bellardi et al., 2007 Digitalis lutea Yellow foxglove Yellow fowglow 16SrI-B Italy Bellardi and Bertaccini, 2005 yellows Digitalis purpurea Foxglove Foxglove yellows 16SrXII-A Serbia Pavlovi et al., 2014a Rehmannia glutinosa Chinese foxglove Rehmannia 16SrI-B Czech Republic P ibylová et al., 2001 proliferation ć ř Solanaceae Capsicum annuum Chili Chili yellows 16SrI, 16SrII India, Indonesia Khan and Raj, 2006; Harling et al., 2009 Cyphomandra betaceum Tamarillo Tamarillo yellows 16SrII Indonesia Harling et al., 2009 Datura inoxia Downy thorn-apple Datura little leaf 16SrVI India Raj et al., 2009b Datura stramonium Common thorn- Datura witches’ 16SrVI, 16SrXII-A India, Czech Republic, Fialová et al., 2009; Özdemir et al., 2009; apple broom Greece, Turkey Lotos et al., 2013; Singh et al., 2013a, 2013b; Singh and Upadhyaya, 2013, 2015 Nicotiana tabacum Tobacco Tobacco “stolbur” 16SrXII-A Europe Seemüller et al., 1998; Marcone, 2011; Mitrovi et al., 2013 Nicotiana tabacum Tobacco Tobacco big bud 16SrII Australia Schneider et al., 1999 Solanum malacoxylon Waxyleaf Waxyleaf nightshade 16SrXII-A Italy Iriti et alć., 2008 nightshade “stolbur” Solanum nigrum Black nightshade Unnamed 16SrII-E, 16SrIX-C Europe, Lebanon Battle et al., 2000; Tolu et al., 2006; Casati et al., 2016 Withania somnifera Indian ginseng Withania witches’ 16SrVI, 16SrI India Zaim and Samad, 1995; Khan et al., 2006; broom Samad et al., 2006 Tamaricaceae Tamarix chinensis Salt cedar Salt cedar witches’ 16SrXXX (‘Ca. P. China Zhao et al., 2005, 2009 broom tamaricis’) Theaceae Camellia japonica Camellia Camellia yellows 16SrV-B China Gao et al., 2015b Journal of Plant Pathology (2016), 98 (3), 379-404 Marcone et al. 391

Table 1 (continued). Phytoplasma diseases of medicinal and aromatic plants.

Tiliaceae Tilia platyphyllos var. Large-leaved linden Linden laciniated leaf 16SrI-B Lithuania Jomantiene et al., 2013 laciniata Tilia platyphyllos var. Large-leaved linden Linden laciniated leaf 16SrI-(L/L)V Lithuania Jomantiene et al., 2013 laciniata witches’ broom Turneraceae Turnera ulmifolia Yellow alder Turnera witches’ 16SrXIII Brazil Montano et al., 2011b broom Ulmaceae Ulmus minor European field elm Elm yellows 16SrV-A (‘Ca. P. ulmi’) Europe, North America Marcone, 2015 (syn. Ulmus campestris) Urticaceae Urtica dioica Nettle Nettle yellows 16SrXII-A, 16SrII Europe, Israel Langer and Maixner, 2004; Bellardi and Bertaccini, 2005; Aryan et al., 2014; Dafny Yelin et al., 2015; Mori et al., 2015; Sabaté et al., 2015; Kosovac et al., 2016 Parietaria officinalis Upright pellitory Pellitory yellows 16SrXII-A, 16SrX Italy Bellardi et al., 2004, 2008; Bellardi and Bertaccini, 2005 Parietaria judaica Spreading pellitory Pellitory yellows 16SrXII-A, 16SrX Italy Bellardi et al., 2004, 2008; Bellardi and Bertaccini, 2005 Valerianaceae Valeriana officinale Valerian Valerian yellows 16SrI-A, M, 16SrXII-A Canada, Lithuania, Hwang et al., 1977b; Khadhair et al., Serbia 2008; Lee et al., 2004; Mitrovi et al., 2013

Verbenaceae ć Verbena x hybrida Vervain Verbena yellows 16SrI-B Turkey P ibylová et al., 2015 Vitex agnus-castus Chaste tree Unnamed 16SrII Europe, Israel Dafny Yelin et al., 2015; Kosovac et al., 2016ř Vitaceae Ampelopsis Porcelain vine Porcelain vine 16SrI Korea Jung et al., 2003 brevipedunculata witches’ broom Vitis vinifera Grapevine Grapevine yellows 16SrXII-A (‘Ca. P. Europe, USA, Australia, Bertaccini et al., 1995b; Padovan et al., solani’); 16SrXII-B (‘Ca. Israel, Chile, Tunisia, 1995; Davis et al., 1997b, 2015; M’hirsi et P. astraliense’); 16SrV-C, Iran, South Africa al., 2004; Belli et al., 2010; Bertaccini et -D; 16SrVII-A (‘Ca. P. al., 2014; Salehi et al., 2016b fraxini’-related); 16SrIX-C; 16SrX-B; 16SrIII-A (‘Ca. P. pruni’-related); 16SrIII-I, -J; 16SrI-A, -B, -C; 16SrII-D

a 16Sr group and subgroup designation according to Davis et al. (2016) and Zhao and Davis (2016), based on computer-simulated RFLP analysis. N.D., not determined.

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