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<I>Phymatotrichopsis Omnivora</I>

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Persoonia 22, 2009: 63 –74 www.persoonia.org RESEARCH ARTICLE doi:10.3767/003158509X430930 Molecular systematics of the cotton root rot pathogen, Phymatotrichopsis omnivora S.M. Marek1, K. Hansen2, M. Romanish3, 4, R.G. Thorn3 Key words Abstract Cotton root rot is an important soilborne disease of cotton and numerous dicot plants in the south-western United States and Mexico. The causal organism, Phymatotrichopsis omnivora (= Phymatotrichum omnivorum), is Ozonium known only as an asexual, holoanamorphic (mitosporic) fungus, and produces conidia resembling those of Botrytis. Pezizales Although the corticoid basidiomycetes Phanerochaete omnivora (Polyporales) and Sistotrema brinkmannii (Cantharel­ Phylogeny lales; both Agaricomycetes) have been suggested as teleomorphs of Phymatotrichopsis omnivora, phylogenetic Phymatotrichum root rot analyses of nuclear small- and large-subunit ribosomal DNA and subunit 2 of RNA polymerase II from multiple Pulchromyces fimicola isolates indicate that it is neither a basidiomycete nor closely related to other species of Botrytis (Sclerotiniaceae, rDNA Leotiomycetes). Phymatotrichopsis omnivora is a member of the family Rhizinaceae, Pezizales (Ascomycota: RPB2 Pezizomycetes) allied to Psilopezia and Rhizina. Texas Article info Received: 29 May 2008; Accepted: 23 February 2009; Published: 11 March 2009. INTRODUCTION Taxonomy The confused taxonomic history of the cotton root rot fungus A devastating disease of cotton in Texas, which caused large goes back more than a century. The causal agent was first numbers of plants in affected areas to suddenly wilt and die, identified by W.G. Farlow as Ozonium auricomum Link, based was first reported in the 1880s (Pammel 1888, 1889). The on nonsporulating mycelium associated with diseased roots disease has been variably called cotton root rot (after the (Pammel 1888). However, this name now applies to the asexual major crop host), Texas root rot (for the centre of distribution), state of Coprinellus (Coprinus) domesticus and related species or Ozonium or Phymatotrichum root rot (for the former names of the causal organism). It has since remained a considerable (Shear 1907, Orton & Watling 1979, Redhead et al. 2001). economic concern, causing up to $ 100 million in annual losses The cotton root rot fungus was described as a new species of to the US cotton crop alone (based on disease loss estimates Ozonium, O. omnivorum Shear (1907), again based on non- and price data for 1980–2008; provided by the National Cotton sporulating mycelium associated with diseased roots. Later, a Council of America, www.cotton.org). The average loss of raw conidial stage was found forming sporemats on soil surrounding cotton fibre yield has been estimated to be 3.5 % in Texas and diseased plants and was named Phymatotrichum omnivorum 2.2 % in Arizona, with losses ranging from 8–13 % in severely (Shear) Duggar (1916). infested areas (Kenerley & Jeger 1992). The causal agent is A hydnoid homobasidiomycete fruiting body was found asso- a soilborne fungus known as Phymatotrichopsis omnivora ciated with diseased plants and named Hydnum omnivorum or, more commonly, Phymatotrichum omnivorum (Streets & Shear (1925), once again based on a different type specimen Bloss 1973, Kenerley & Jeger 1992, Kirkpatrick & Rothrock (C.L. Shear 5267, BPI 259732) from that of Ozonium om­ 2001; see below for taxonomic authorities). This species is nivorum or Phymatotrichum omnivorum. Later, a corticioid capable of infecting more than 2 000 species of dicots (Streets homobasidiomycete fruiting body was discovered in a culture & Bloss 1973), arguably the largest host range of any plant of Phymatotrichum omnivorum and identified as Sistotrema pathogen. It also causes severe losses in alfalfa, vegetable brinkmannii (Baniecki & Bloss 1969). Basidiospores of the crops, grapes, and fruit and nut orchards throughout its range, Sistotrema failed to form the mycelium of Phymatotrichum, and which stretches from eastern Texas and southern Oklahoma Weresub & LeClair (1971) considered this report to be based west through Arizona and south into Mexico (Streets & Bloss on a homothallic culture contaminant. 1973). Generally, infected plants quickly wilt in the summer, and almost inevitably die, usually in large circular patches The type species of Phymatotrichum, P. gemellum Bonord., in the field (Fig. 1a, b). Below ground, the taproots of wilted was shown to be a member of Botrytis by Hennebert (1973). plants are rotted and usually covered with mycelial strands of Hennebert (1973) believed that the name Phymatotrichum the causal fungus (Fig. 1c). omnivorum should be attributed to Duggar alone since it was based on different specimens than examined by Shear (1907) 1 Department of Entomology and Plant Pathology, 127 Noble Research when he described Ozonium omnivorum, and because the Center, Oklahoma State University, Stillwater, OK 74078-3033, USA. 2 Harvard University Herbaria, 22 Divinity Ave., Cambridge, MA 02138, distinguishing features described by Duggar (the conidia) USA; Present address: Swedish Museum of Natural History, Department were not present in the type of Ozonium omnivorum (C.L. of Cryptogamic Botany, P.O. Box 50007, 104 05 Stockholm, Sweden. Shear 1447, BPI 455660). Phymatotrichum omnivorum was 3 Department of Biology, University of Western Ontario, London, Ontario, transferred to Phymatotrichopsis omnivora (Duggar) Hennebert N6A 5B7, Canada; corresponding author e-mail: [email protected]. 4 Present address: Department of Medical Genetics, University of British and Phymatotrichum fimicola Dring to Pulchromyces fimicola Columbia, Vancouver, BC, V5Z 1L3, Canada. (Dring) Hennebert. © 2009 Nationaal Herbarium Nederland & Centraalbureau voor Schimmelcultures You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 64 Persoonia – Volume 22, 2009 3 -tub – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – β . RPB2 DQ470918 – – – AY641054 – AY500504 DQ247787 – – – DQ497613 – – – – – – – – – – – DQ470892 – – – DQ470891 AY641045 – – – – – – AF107810 – – DQ247785 – – DQ471123 – – – – AY500506 – – – – – – – bold LSU DQ168334 U42673 U42680 AF335118 AY544664/AF279398 U42684 AY500531 DQ247799 U42686 DQ220344 DQ220342 AY544655 AY544660 AY500526 DQ168335 – U42683 AY500530 U42694 AY307944 AY945860 AY945854 U42678 U42670/AY544667 DQ220329 AY945850 – AY544673 U42675 U42676 DQ062995 DQ167411 U42674 AF335120 AY500539 U42667/AY544665 DQ220374 AF279401 AY544654 AY500527 – AY544661 U42688 DQ168336 DQ220351 DQ220353 AY500534 U42689 DQ220358 DQ220363 AY500536 DQ646524 DQ220371 DQ220377 GenBank Accession Numbers GenBank ITS – – – – – – – – – – – – – – – – – – – – – – – – – – –,DQ220335 – – – – – – – – – – – – – – – – – – – – – – – – – – – SSU DQ062997 U42646 U42653 DQ646530 U42642/AY544708 U42657 Z30241 DQ247807 U42659 DQ646527 DQ646528 AY544699 AY544704 AY544720 – U53372 U42656 – U42666 AF104340 AF006311 AF104341 U42651 U42643/AY544711 AF104342 AF004948 DQ646526 AY544717 U42648 U42649 DQ063000 DQ646532 U42647 DQ646535 DQ646536 U42641/AY544709 AF006314 Z27393 AY544698 AY544721 U53373 AY544705 U42661 AF104665 DQ062996 DQ646529 U53380 U42662 DQ646531 DQ646533 DQ646534 DQ646537 DQ646538 AF061720 2 ) 1 CBS 626.71 1889 (OSC) JMT NSW 7196 (OSC) (FH) 18510 PAN 10968 ATCC 22335, SSU+LSU: MV3 (dubl. OSC 100041), LSU+RPB2: SSU: NRRL RF 533 (OSC) SSU: UME 29218, LSU: KS-94-4 (C) DJ053103-2 12617 (OSC) JMT KH.03.61 (FH) Trappe 18034 (FH, dubl. OSC) Trappe OSC 100019 (OSC) Vouchers, Isolates, Strains (Herbarium Vouchers, OSC 100026 KH 00.008 (C) (dubl. OSC 100079) CBS 389.68 RK 95.55 (O) 13020 (OSC) JMT Rana 79.049 (C) 12993 (OSC) JMT Keller & K.C. Rudy s.n. (FH) SSU: mh 694 (FH), LSU: H.W. SSU: mh 686 (FH), LSU: 1D-D5 (FH) (FH), LSU: RK 95.12 (Herb. Roy Kristiansen) SSU: ‘Norway’ NSW 4498 (MICH) 22213) OSC 100045 (dubl. NRRL mh 669 (FH) mh 101 (FH) (FH, dubl. OSC) 11775 Trappe OSC 100068 20925 (dubl. CBS 335.73) NRRL NSW 6494 (OSC) CBS 344.73 KS-94-005 (C) 7205 (OSC) JMT All-94-8 (C) KH.01.06 (C) 22447 (dubl. OSC 100042) 25405, SSU+LSU: NRRL SSU+LSU+RPB2: NRRL mh PR61 (FH) 176 (F) SSU: UME 29192 (U), LSU: JP OSC 100018 KH.02.005 (C) (dubl. OSC 100082) ARON 2167 (O) KH04282003-4 (dubl. OSC 100034) 7014 (OSC) JMT SSU: _ (FH), LSU: C F-49793 (C) PR-5954 (FH) KH.03.100 (FH) 00.027 (C) ARON 2102, LSU+RPB2: JHP SSU: 14825 (OSC) JMT KH.03.54 (FH) CBS 782.70 KH.00.07 (C) KH.03.43 (FH) KH.03.156 (FH) ARON 2690 (U), LSU: KH.03.55 (FH) SSU: gilkeyae s f. cervina sp. compressa Species used in molecular phylogenetic analyses, specimen information and GenBank accession numbers. New sequences generated for this study are indicated with GenBank numbers in sp. cf. cf. Table 1 Table Aleuria aurantia Anthracobia Ascobolus carbonarius Ascobolus crenulatus Ascodesmis nigricans Ascodesmis sphaerospora Balsamia magnata Barssia oregonensis
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  • The Phylogeny of Plant and Animal Pathogens in the Ascomycota

    The Phylogeny of Plant and Animal Pathogens in the Ascomycota

    Physiological and Molecular Plant Pathology (2001) 59, 165±187 doi:10.1006/pmpp.2001.0355, available online at http://www.idealibrary.com on MINI-REVIEW The phylogeny of plant and animal pathogens in the Ascomycota MARY L. BERBEE* Department of Botany, University of British Columbia, 6270 University Blvd, Vancouver, BC V6T 1Z4, Canada (Accepted for publication August 2001) What makes a fungus pathogenic? In this review, phylogenetic inference is used to speculate on the evolution of plant and animal pathogens in the fungal Phylum Ascomycota. A phylogeny is presented using 297 18S ribosomal DNA sequences from GenBank and it is shown that most known plant pathogens are concentrated in four classes in the Ascomycota. Animal pathogens are also concentrated, but in two ascomycete classes that contain few, if any, plant pathogens. Rather than appearing as a constant character of a class, the ability to cause disease in plants and animals was gained and lost repeatedly. The genes that code for some traits involved in pathogenicity or virulence have been cloned and characterized, and so the evolutionary relationships of a few of the genes for enzymes and toxins known to play roles in diseases were explored. In general, these genes are too narrowly distributed and too recent in origin to explain the broad patterns of origin of pathogens. Co-evolution could potentially be part of an explanation for phylogenetic patterns of pathogenesis. Robust phylogenies not only of the fungi, but also of host plants and animals are becoming available, allowing for critical analysis of the nature of co-evolutionary warfare. Host animals, particularly human hosts have had little obvious eect on fungal evolution and most cases of fungal disease in humans appear to represent an evolutionary dead end for the fungus.
  • A Case of the Yellow Morel from Israel Segula Masaphy,* Limor Zabari, Doron Goldberg, and Gurinaz Jander-Shagug

    A Case of the Yellow Morel from Israel Segula Masaphy,* Limor Zabari, Doron Goldberg, and Gurinaz Jander-Shagug

    The Complexity of Morchella Systematics: A Case of the Yellow Morel from Israel Segula Masaphy,* Limor Zabari, Doron Goldberg, and Gurinaz Jander-Shagug A B C Abstract Individual morel mushrooms are highly polymorphic, resulting in confusion in their taxonomic distinction. In particu- lar, yellow morels from northern Israel, which are presumably Morchella esculenta, differ greatly in head color, head shape, ridge arrangement, and stalk-to-head ratio. Five morphologically distinct yellow morel fruiting bodies were genetically character- ized. Their internal transcribed spacer (ITS) region within the nuclear ribosomal DNA and partial LSU (28S) gene were se- quenced and analyzed. All of the analyzed morphotypes showed identical genotypes in both sequences. A phylogenetic tree with retrieved NCBI GenBank sequences showed better fit of the ITS sequences to D E M. crassipes than M. esculenta but with less than 85% homology, while LSU sequences, Figure 1. Fruiting body morphotypes examined in this study. (A) MS1-32, (B) MS1-34, showed more then 98.8% homology with (C) MS1-52, (D) MS1-106, (E) MS1-113. Fruiting bodies were similar in height, approxi- both species, giving no previously defined mately 6-8 cm. species definition according the two se- quences. Keywords: ITS region, Morchella esculenta, 14 FUNGI Volume 3:2 Spring 2010 MorchellaFUNGI crassipes Volume, phenotypic 3:2 Spring variation. 2010 FUNGI Volume 3:2 Spring 2010 15 Introduction Materials and Methods Morchella sp. fruiting bodies (morels) are highly polymorphic. Fruiting bodies: Fruiting bodies used in this study were collected Although morphology is still the primary means of identifying from the Galilee region in Israel in the 2003-2007 seasons.
  • Notes on British Species of Byssonectria

    Notes on British Species of Byssonectria

    Mycol. Res 100 (7). 881-882 (1996) Prmled in Greal Bnlam 881 Notes on British species of Byssonectria Y.-J. YA01,2 AND B. M. SPOONERl 1 Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE, UK 2 School of Biomolecular Sciences, Liverpool John Moores UnIVerslly, Byrom Street, LIverpool L3 3Ar, UK Notes on the taxonomy of the species reported from Britain as Byssonectria and Inermisia are presented. Two species, B. fusispora and B. terrestris, are retained in the British list, although fresh collections are required to confirm the distinction between them. Byssoneetna tetraspora and Inermisia pi/ifera should be placed in Oetospora. Observations on the type of O. pi/ifera are provided to update the species description. Byssonectria P. Karst., originally referred to the Hypocreales cyanobacteria grow, and in having larger ascospores (24'0• Lindau, was shown by Korf (1971) to be an earlier name for 29'0 x 7'0-II'0 I-lm). The subiculum is, in fact, variable Inermisia Rifai (Rifai, 1968). The genus has been distinguished amongst British collections previously named as either B. from Octospora Hedw. on the basis of excipular structure, and fusispora or Peziza aggregata, ranging from very conspicuous to the non-bryophilous (Benkert, 1987) or nitrogen-rich (Pfister, scanty or even absent. Such variation is seen especially in 1993) habitat, although Khare & Tewari (1978) treated these those collections from plant debris; collections on soil rarely names as synonyms. exhibit development of a subiculum. This may imply that the Three accepted names in Byssonectria and Inermisia, B. development of subiculum is related to the substrate.