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AR TICLE the Inclusion of Downy Mildews in a Multi-Locus-Dataset

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AR TICLE the Inclusion of Downy Mildews in a Multi-Locus-Dataset GRLLPDIXQJXV IMA FUNGUS · VOLUME 2 · NO 2: 163–171 The inclusion of downy mildews in a multi-locus-dataset and its reanalysis ARTICLE reveals a high degree of paraphyly in Phytophthora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bstract: 3DWKRJHQVEHORQJLQJWRWKHOomycota, a group of heterokont, fungal-like organisms, are amongst the Key words: PRVWQRWRULRXVSDWKRJHQVLQDJULFXOWXUH,QSDUWLFXODUWKHREOLJDWHELRWURSKLFGRZQ\PLOGHZVDQGWKHKHPLELRWURSKLF $8WHVW members of the genus Phytophthora are responsible for a huge variety of destructive diseases, including sudden downy mildews oak death caused by P. ramorum, potato late blight caused by P. infestans, cucurbit downy mildew caused by multigene phylogeny Pseudoperonospora cubensis, and grape downy mildew caused by Plasmopara viticola$ERXWVSHFLHVRI Peronosporaceae GRZQ\PLOGHZVDQGURXJKO\VSHFLHVRIPhytophthora are currently accepted, and recent studies have revealed Phytophthora WKDW WKHVH JURXSV DUH FORVHO\ UHODWHG +RZHYHU WKH GHJUHH WR ZKLFK Phytophthora is paraphyletic and where taxonomy exactly the downy mildews insert into this genus in relation to other clades could not be inferred with certainty to GDWH+HUHZHSUHVHQWDPROHFXODUSK\ORJHQ\HQFRPSDVVLQJDOOFODGHVRIPhytophthora as represented in a multi- ORFXVGDWDVHWDQGWZRUHSUHVHQWDWLYHVRIWKHPRQRSK\OHWLFGRZQ\PLOGHZVIURPGLYHUJHQWJHQHUD2XUUHVXOWV demonstrate that PhytophthoraLVDWOHDVWVL[WLPHVSDUDSK\OHWLFZLWKUHVSHFWWRWKHGRZQ\PLOGHZV7KHGRZQ\ PLOGHZUHSUHVHQWDWLYHVDUHFRQVLVWHQWO\QHVWHGZLWKLQFODGH FRQWDLQVPhytophthora palmivora ZKLFKLVSODFHG VLVWHUWRFODGH FRQWDLQVPhytophthora infestans 7KLV¿QGLQJZRXOGHLWKHUQHFHVVLWDWHSODFLQJDOOGRZQ\PLOGHZV and Phytopthora species in a single genus, either under the oldest generic name Peronospora or by conservation the later name Phytophthora, or the description of at least six new genera within Phytophthora7KHFRPSOLFDWLRQV of both options are discussed, and it is concluded that the latter is preferable, as it warrants fewer name changes DQGLVPRUHSUDFWLFDO Article info:6XEPLWWHG6HSWHPEHU$FFHSWHG2FWREHU3XEOLVKHG1RYHPEHU INTRODUCTION *|NHU et al 7KLQHV et al. 7KLQHV 7KH FORVH UHODWLRQVKLS RI WKH GRZQ\ PLOGHZV DQG 2RP\FHWHV DUH D JURXS RI RUJDQLVPV WKDW VXSHU¿FLDOO\ Phytophthora revealed by these studies is in contrast to the resemble fungi in their hyphal growth and absorptive way of ZLGHO\ XVHG WD[RQRPLF FODVVL¿FDWLRQV RI :DWHUKRXVH QXWULWLRQ +RZHYHU WKH\ DUH QRW FORVHO\ UHODWHG WR Mycota, DQG 'LFN LQ ZKLFK Phytophthora and Pythium but belong to a group of heterokont organisms, Straminipila were grouped together in the family Pythiaceae $OWKRXJK 'LFN ZKLFK DOVR LQFOXGHV GLDWRPV DQG VHDZHHGV &RRNHet al LQIHUUHGDSRVLWLRQRIPeronospora sparsa 2RP\FHWHVKDYHDGDSWHGWRSDUDVLWLVPRISODQWVDWOHDVWWKUHH DVDVLVWHUJURXSRIFODGH DVGH¿QHGLQWKDWVWXG\ EDVHGRQ times, once in the Saprolegniales in the genera Aphanomyces ,76VHTXHQFHVDORQHQRVXEVWDQWLDOSK\ORJHQHWLFUHVROXWLRQ and Pachymetra 5LHWKPOOHUet al.'LpJXH]8ULEHRQGR was present on the phylogenetic backbone, thus failing to et al DQGVHSDUDWHO\LQAlbuginales and Peronosporales position this group within the genus Phytophthora 2WKHU 5LHWKPOOHUet al. +XGVSHWKet al. 7KLQHVet al VWXGLHV LQFOXGLQJPXOWLORFXVVWXGLHV WKDWLQFOXGHGERWKGRZQ\ :KLOHWKHHYROXWLRQRIREOLJDWHELRWURSK\VHHPVWREH mildew and Phytophthora species have so far not resolved the DQ DQFLHQW RFFXUUHQFH IRU WKH ZKLWH EOLVWHU UXVWV 7KLQHV placement of downy mildews in relation to the different clades .DPRXQ WKHGRZQ\PLOGHZVKDYHPRUHUHFHQWO\DULVHQ of Phytophthora 5LHWKPOOHU et al *|NHU et al from PhytophthoraOLNH DQFHVWRUV 5LHWKPOOHU et al 7KLQHVet al.*LUHVVHet al. $GGLWLRQDOO\7KLQHVet © 2011 International Mycological Association You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: <RXPXVWDWWULEXWHWKHZRUNLQWKHPDQQHUVSHFL¿HGE\WKHDXWKRURUOLFHQVRU EXWQRWLQDQ\ZD\WKDWVXJJHVWVWKDWWKH\HQGRUVH\RXRU\RXUXVHRIWKHZRUN Non-commercial: <RXPD\QRWXVHWKLVZRUNIRUFRPPHUFLDOSXUSRVHV No derivative works: <RXPD\QRWDOWHUWUDQVIRUPRUEXLOGXSRQWKLVZRUN For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. VOLUME 2 · NO. 2 163 Runge et al. al GHPRQVWUDWHGWKDWWKHVXSSRUWIRUWKHVLVWHUJURXS FRPSXWHUSDFNDJHY /DVHUJHQH0DGLVRQ:, DQGZHUH relationship of PeronosporaDQGFODGHLQIHUUHGE\&RRNHet DOLJQHGVHSDUDWHO\XVLQJ0$))7Y .DWRKet al al FRXOGKDYHEHHQWKHUHVXOWRIDQDOLJQPHQWDUWHIDFW XVLQJ D ZHEVHUYHU LQWHUIDFH KWWSZZZJHQRPHMSWRROV &RQYHUVHO\DUHFHQWVWXG\E\%ODLUet al DGGUHVVHGWKH PDIIW 7KH*,16LDOJRULWKPZDVFKRVHQIRUDOODOLJQPHQWV phylogenetic relationships of Phytophthora species with good 6XEVHTXHQWO\ WKH DOLJQHG VHTXHQFHV ZHUH FRQFDWHQDWHG ARTICLE resolution, but no downy mildew was included in that study, for phylogenetic analyses and no further editing was done OHDYLQJWKHLUSODFHPHQWWRVSHFXODWLRQ'RZQ\PLOGHZVKDYH on the alignment to ensure reproducibility and to prevent EHHQ VKRZQ WR EH D PRQRSK\OHWLF DVVHPEODJH E\ *|NHU et LQWURGXFWLRQRIELDV$IWHUWKHUHPRYDORIOHDGLQJDQGWUDLOLQJ al. +RZHYHU*|NHU 6WDPDWDNLV ODWHU LQVSLWH JDSVQXFOHRWLGHVLWHVZHUHLQFOXGHGLQWKHSK\ORJHQHWLF RIEHLQJSXEOLVKHGHDUOLHUWKDQ*|NHUet al. FDPHWRWKH DQDO\VHV7KHVHFRPSULVHGVHYHQORFLESRIWKHEHWD conclusion that a placement of PhytophthoraFODGHZLWKLQWKH WXEXOLQJHQHESRIWKH6ULERVRPDOSURWHLQ/JHQH downy mildews would also be possible, although no support ESRIWKHWUDQVODWLRQHORQJDWLRQIDFWRUDOSKDJHQH FRXOG EH REWDLQHG IRU WKLV VFHQDULR 7KH TXHVWLRQ RI ZKLFK ESRIWKH6QXFOHDU ULERVRPDO'1$JHQH ESRIWKH is the sister clade of the downy mildews, and how this clade JO\FHUDOGHK\GHSKRVSKDWHGHK\GURJHQDVHJHQHES is embedded among the different lineages of Phytophthora RIWKHKHDWVKRFNSURWHLQJHQHDQGESRIWKHHQRODVH therefore continues to be controversial, but is fundamental for JHQH7KHDOLJQPHQWWRJHWKHUZLWKWKHWUHHIURPWKH%D\HVLDQ understanding the evolution of this group of important plant $QDO\VLVVKRZQLQ)LJKDVEHHQGHSRVLWHGLQ7UHH%$6( SDWKRJHQVHVSHFLDOO\ZLWKUHVSHFWWRWKHHYROXWLRQRIELRWURSK\ ZZZWUHHEDVHRUJ XQGHUWKHDFFHVVLRQQXPEHU6 In addition, the taxonomic status of many Phytophthora 7KHJHQHUDOWLPHUHYHUVLEOH *75 PRGHOZDVVHOHFWHGIRU VSHFLHVGHSHQGVRQWKHGHJUHHRISDUDSK\O\RIWKHJHQXV$W WKHFRQFDWHQDWHGDOLJQPHQWXVLQJ0RGHOWHVWY 3RVDGD OHDVWZLWKWZRFODGHVDQGPhytophthora is paraphyletic &UDQGDOO DQG3$83YE 6ZRIIRUG ZLWK ZLWKUHVSHFWWRGRZQ\PLOGHZV &RRNHet al*|NHUet al. JDPPDGLVWULEXWHG VXEVWLWXWLRQ UDWHV VKDSH SDUDPHWHU 7KLQHVet al EXWVRIDUWKHGHJUHHRISDUDSK\O\ DQG SURSRUWLRQ RI LQYDULDEOH VLWHV SLQY 7KH of Phytophthora FRXOG QRW EH UHVROYHG 7KHUHIRUH LW ZDV YDOXHV RI WKHVH SDUDPHWHUV ZHUH LQFOXGHG LQ WKH %D\HVLDQ the aim of this study to resolve the phylogenetic placement DQG0LQLPXP(YROXWLRQDQDO\VHV RIWKHPRQRSK\OHWLFGRZQ\PLOGHZV UHSUHVHQWHGE\WKHWZR 0LQLPXP(YROXWLRQ 0( DQDO\VLVZDVGRQHXVLQJ0(*$ divergent downy mildew genera for which genome data are Y 7DPXUD et al. ZLWK WKH JDPPDGLVWULEXWHG FXUUHQWO\ DYDLODEOH DPRQJ Phytophthora and to test this VXEVWLWXWLRQ UDWHV DV LQIHUUHG E\ 0RGHOWHVW DQG XVLQJ placement statistically, to further clarify the relationships within WKH 0D[LPXP&RPSRVLWH/LNHOLKRRG VXEVWLWXWLRQ PRGHO WKLVJURXSRILPSRUWDQWSODQWSDWKRJHQV )RU LQIHUULQJ WUHH UREXVWQHVV ERRWVWUDS UHSOLFDWHV )HOVHQVWHLQ ZHUHFRPSXWHG )RU 0D[LPXP /LNHOLKRRG 0/ LQIHUHQFH WKH 5$[0/ MATERIALS AND METHODS ZHEVHUYHU DW KWWSSK\OREHQFKYLWDOLWFKUD[POEE 6WDPDWDNLV et al ZDV XVHG ZLWK VWDQGDUG VHWWLQJV $OOVHTXHQFHVRIPhytophthora and Pythium were obtained and maximum likelihood search, including an estimation of IURPWKHVWXG\RI%ODLUet al DYDLODEOHLQWKH1DWLRQDO LQYDULDEOH VLWHV7KH DQDO\VLV ZDV UHSHDWHG ¿YH WLPHV ZLWK &HQWHU IRU %LRWHFKQRORJ\ ,QIRUPDWLRQ 1&%, QXFOHRWLGH ERRWVWUDSUHSOLFDWHVHDFK7KHERRWVWUDSVXSSRUWYDOXHV GDWDEDVH *HQ%DQN 7KH GDWDVHW LQFOXGHV VHTXHQFHV RI obtained were averaged, because the rapid bootstrapping seven different loci, and all species for which all seven loci DOJRULWKPFDQOHDGWRVRPHGHYLDWLRQ were not available were discarded, except for two Pythium )RU%D\HVLDQDQDO\VLV0U%D\HV +XHOVHQEHFN 5RQTXLVW VSHFLHVIRUZKLFKRQO\VL[RIWKHVHYHQORFLFRXOGEHREWDLQHG DWWKH3K\OHPRQZHEVHUYHU KWWSSK\OHPRQELRLQIR 7KLVUHVXOWHGLQDQRYHUDOOGDWDVHWRIVSHFLHVVDPSOHG FLSIHV DQG DW D ORFDO VHUYHU IRU SDUDOOHO UXQV ZDV XVHG 7KHVHTXHQFHVRIPhytophthora infestans were used to obtain )RXU LQFUHPHQWDOO\ KHDWHG VLPXOWDQHRXV 0DUNRY &KDLQ homologous sequences from the genome of Hyaloperonspora 0RQWH&DUORFKDLQVZHUHUXQIRUWZRPLOOLRQJHQHUDWLRQVZLWK arabidopsidisIURPWKH1&%,GDWDEDVHXVLQJ%/$67 $OWVFKXO HYHU\th tree sampled, under the general time reversible et al DQG IURP WKH JHQRPH RI Pseudoperonospora *75 PRGHO ZLWK WKH JDPPDGLVWULEXWHG VXEVWLWXWLRQ UDWHV cubensis 7LDQ et al XVLQJ WKH DQQRWDWHG (67 DQG SURSRUWLRQ RI LQYDULDEOH VLWHV DV LQIHUUHG E\ 0RGHOWHVW VHTXHQFHLQIRUPDWLRQ%HFDXVHQRVHTXHQFHLQIRUPDWLRQIRU
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