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Phytoplasma Identity and Disease Etiology Symposium New Perspectives on Phytopathogenic Mollicutes Phytoplasma Identity and Disease Etiology R. E. Davis and W. A. Sinclair First author: Molecular Plant Pathology Laboratory, Agricultural Research Service-USDA, Beltsville, MD 20705; second author: Department of Plant Pathology, Cornell University, Ithaca, NY 14853-4203. Accepted for publication 18 September 1998. ABSTRACT Davis, R. E., and Sinclair, W. A. 1998. Phytoplasma identity and disease reflect specificities in transmission by vectors and vector feeding prefer- etiology. Phytopathology 88:1372-1376. ences; phytoplasma-insect vector relationships are keys to understanding evolutionary divergence of phytoplasma lineages; small differences in a Many plant diseases believed to be caused by phytoplasmas were de- highly conserved phytoplasma gene may be regarded as potential indica- scribed before phytoplasma groups were delineated through molecular tors of separate gene pools; the reliability of a diagnosis based on symp- analyses. It is now possible to assess the relationships between phyto- toms must be learned empirically (i.e., through case study for each syn- plasma identity or classification and specific plant diseases. Data were drome); and some discrete diseases can be ascribed to phytoplasma taxa consistent with the hypothesis of a common ancestral origin of patho- at the 16S rRNA group level, whereas others are clearly associated with genicity genes in many phytoplasmas and a limited repertoire of plant phytoplasma taxa below this level. responses to certain pathogen signals. Observations also were consistent with the hypotheses that the botanical host ranges of some phytoplasmas Additional keywords: evolution, mycoplasmalike organism, taxonomy. In plant pathology, as in human and animal medicine, not only natural infections by mixed phytoplasma populations (2,3,15,24) pathogens but also the diseases they cause historically have been can hamper disease diagnosis and complicate attribution of a dis- named largely on the basis of symptoms exhibited by infected hosts. ease to a single phytoplasma taxon. Plant diseases attributed to phytoplasmas are no exception to this In this paper, we present a brief assessment of the relationship practice. For example, many phytoplasmal diseases have been classi- between classification of phytoplasmas and differentiation of their fied in general terms, either as decline or virescence diseases. Dis- associated plant diseases. These considerations are important for ease names, such as aster yellows, strawberry multiplier, pear de- understanding phytoplasma biology and for successful disease man- cline, palm lethal yellows, and others, indicate the importance of agement and regulation of interregional and international shipment perceived symptoms in the assignment of common names to dis- of plants that potentially harbor phytoplasmas. eases. Indeed, common names of pathogens are derived from the names of plant diseases with which they are first associated. PHENOTYPIC CHARACTERS AND Studies of phytoplasmal disease etiology usually have proceeded PHYTOPLASMA CLASSIFICATION under the presumption that specific phytoplasmas cause specific diseases. This concept was established even before putative phyto- Because phytoplasmas cannot yet be isolated in pure culture in plasma taxa were differentiated and proved correct for some dis- vitro, phenotypic characters useful for identification and classifi- eases (e.g., apple proliferation, ash yellows, and elm yellows [31, cation have been difficult to determine. Molecular characterization 41,43]). However, it has become clear that different phytoplasmas of conserved genes has presented a partial solution to the problem, can cause apparently identical symptoms in certain plants, includ- enabling the construction of a classification scheme that is inde- ing phytoplasmas associated with grapevine yellows, bigbud of pendent of phenotypic characters. Several studies of 16S rRNA tomato, and disorders of periwinkle (Catharanthus roseus) (2,6,8, gene sequences have confirmed the appropriate placement of phy- 11,22,38,42). On the other hand, some closely related phyto- toplasmas within the class Mollicutes and have led to recognition plasmas can cause distinctly different symptoms in host plants. of phytoplasmas as a distinct monophyletic clade within the class For example, the syndromes induced by aggressive and nonag- (16). Phytoplasmas have been classified into more than a dozen gressive strains of ash yellows phytoplasmas in experimentally in- groups (Table 1); each group apparently corresponds to at least fected green ash (Fraxinus pennsylvanica) differ dramatically (W. A. one species (also listed in Table 1 of Lee et al. [25]). This concept Sinclair, unpublished data). Closely related strains in a single sub- is supported by studies on genes that encode rRNA, ribosomal cluster (subgroup) of the aster yellows genomic cluster (group) protein, and the elongation factor Tu (8,15–17,19,21,26,29,36,39, can induce either phyllody or small flowers of normal color in in- 41,44). fected periwinkle plants. Such observations and the occurrence of Many plant diseases believed to be caused by phytoplasmas were described before phytoplasma groups were delineated through DNA analyses. It is now possible to assess the relationship be- Corresponding author: R. E. Davis; E-mail address: [email protected] tween phytoplasma identity or classification and specific plant diseases. The presence, absence, or magnitude of a phenotypic Publication no. P-1998-1027-01O character can be assessed for each phytoplasma strain, and phyto- This article is in the public domain and not copyrightable. It may be freely re- printed with customary crediting of the source. The American Phytopathological plasma taxa can be compared for characters, such as plant and Society, 1998. insect host ranges and propensity to induce particular symptoms, 1372 PHYTOPATHOLOGY such as hyperplasia, phyllody, or witches’-brooms. Schneider and TABLE 1. Selected strains of phytoplasmas classified based on restriction fragment Seemüller (40) assessed the molecular classification of phytoplas- length polymorphism or putative restriction site analysis of 16S rRNA gene sequences mas associated with four symptom types on periwinkle. They found 16S rRNA group Source that apart from the virescence-inducing organisms of the aster yel- (subgroup)a Phytoplasma (strain designation) location lows group (sensu lato), there was no consistent relationship between 16SrI (Aster yellows group) symptom type and phytoplasma group identity. Previously, Lee et al. I(A) Tomato big bud (BB) Arkansas (22) determined that different disease symptoms could be induced I(B) Michigan aster yellows (MIAY) Michigan in a host plant by closely related strains classified in the same sub- I(C) Clover phyllody (CPh) Canada cluster (subgroup) in the aster yellows phytoplasma genomic cluster. I(D) Paulownia witches’-broom (PaWB) Taiwan Because descriptions of organisms cultured in vitro are required I(E) Blueberry stunt (BBS1) Michigan I(F) Apricot chlorotic leafroll (ACLR-AY) Spain for naming of species in the class Mollicutes and phytoplasmas I(K) Strawberry multiplier (STRAWB 2) Florida cannot yet be isolated in culture, phytoplasma lineages are being referred to as “Candidatus Phytoplasma species.” Two provisional 16SrII (Peanut witches’-broom group) species have been named: Candidatus Phytoplasma aurantifolia (47) II(A) Peanut witches’-broom (PnWB) Taiwan II(B) Witches’-broom of lime (WBDL), Arabian and Candidatus Phytoplasma australiense (8). These designations, “Candidatus Phytoplasma aurantifolia” Peninsula as well as others that will be assigned based on analysis of 16S II(C) Faba bean phyllody (FBP) Sudan rRNA or other conserved genes, imply that the new taxa are (i) phe- II(D) Sweet potato little leaf (SPLL) Australia notypically distinct and (ii) representative of new lineages. Evidence 16SrIII (X-disease group) for the latter is required for publication of a provisional phytoplasma III(A) X-disease (CX) Canada taxon (34,35). However, phylogenetically distinct phytoplasmas al- III(B) Clover yellow edge (CYE) Canada ready have been found to share some phenotypic characters III(C) Pecan bunch (PB) Georgia (e.g., production of a virescence-inducing factor), while display- III(D) Goldenrod yellows (GR1) New York ing other characters that are unique (e.g., host range or vector III(E) Spirea stunt (SP1) New York III(F) Milkweed yellows (MW1) New York specificity). Thus, the relationship between phytoplasma classifica- III(G) Walnut witches’-broom (WWB) Georgia tion and specific plant diseases and symptoms appears to be only III(H) Poinsettia branch-inducing (PoiBI) United States partially congruent. III(I) Virginia grapevine yellows (VGYIII) Virginia Current phytoplasma classification schemes provide for recog- 16SrIV (Coconut lethal yellows group) nition of subgroups within major phytoplasma groups (8,10,15– IV(A) Coconut lethal yellowing (LY) Florida 17,19,26,39,46). Subgroup designation carries the presumption that IV(B) Tanzanian coconut lethal decline (LDT) Tanzania the subgroup population would be judged phenotypically discrete if its phenotype were known. Presumably, subgroups represent dis- 16rV (Elm yellows group) tinct gene pools that have become discrete through evolution after V(A) Elm yellows (EY1) United States V(B) Cherry lethal yellows (CLY) China isolation from an ancestral population, perhaps by inhabiting dif- V(C) Flavescence dorée (FD) France ferent
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