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