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  (This is a sample cover image for this issue. The actual cover is not yet available at this time.) This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institutionand sharing with colleagues.Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third partywebsites are prohibited.In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further informationregarding Elsevier’s archiving and manuscript policies areencouraged to visit:http://www.elsevier.com/copyright  Author's personal copy Clari 󿬁 cation on rust species potentially infecting pea ( Pisum sativum  L.) cropand host range of   Uromyces pisi  (Pers.) Wint Eleonora Barilli a , * , Ana Moral a , Jose 󿬁 na C. Sillero b , Diego Rubiales a a Institute for Sustainable Agriculture, CSIC, Apdo. 4084, E-14080 Córdoba, Spain b IFAPA, Centro Alameda del Obispo, Apdo. 3092, E-14080 Córdoba, Spain a r t i c l e i n f o  Article history: Received 4 July 2011Received in revised form4 January 2012Accepted 8 January 2012 Keywords: Pea rust Uromyces pisi Host range a b s t r a c t Rust is a serious disease of pea whose casual agent is not always understood. In this paper we studiedreaction of pea accessions to seven rust species infecting closely related legumes,  󿬁 nding that indeed peacan be infected mainly by  Uromyces pisi , followed by  Uromyces viciae-fabae . Other rust species like Uromyces striatus ,  Uromyces ciceris-arietini ,  Uromyces anthyllidis  and  Uromyces vignae  can also infect andreproduce on pea, although in a minor extent. All  U. pisi  isolates tested were very virulent on peaaccessions, but isolates UpPt-03 and UpKeS-05 (from Palmar de Troya, Spain and Kafr-El-Sheik, Egyptrespectively) were signi 󿬁 cantly most infective. In addition to this we studied in detail the host range of  U. pisi  by inoculating multiple accessions of various legumes with urediospores of seven isolates of   U. pisi from different geographical srcins. Both experiments were performed under controlled conditions.Based on the evidence presented here the host range of   U. pisi  is greater than previously recorded,including genotypes belonging to  Cicer arietinum ,  Vicia articulada ,  Vicia ervilia  and  Vicia faba , which werenot mentioned before.   2012 Elsevier Ltd. All rights reserved. 1. Introduction Pea rust is a serious disease of worldwide distribution causingyield losses in pea ( Pisum sativum  L.). In years of epidemics, rustresultsinaffectedleavesdryingupanddetachingfromtheplant,sobeans remain undeveloped and consequently yield losses can bemore than 30% (EPPO, 2010). The pathogen develops in warm,humid weatherand maycause signi 󿬁 cant damagewhen epidemicsstart early in the season and when springs are humid andtemperate (Sillero et al., 2006; Emeran et al., 2008). Most reports refer to  Uromyces viciae-fabae  (Pers.) J. Schröt (syn. Uromyces fabae  Pers de Bary) (Xue and Warkentin, 2001; Singh et al., 2004; Vijayalakshmi et al., 2005; Kushwaha et al., 2006) as the causal agent of pea rust. However, few observations onmorphology or attempts for classi 󿬁 cation are provided in thesereports. It was recently suggested that  Uromyces pisi  (Pers.) Wint. isthe principal agent causing pea rust at least in temperate regions(Barillietal.,2009a),whatisinagreementwithearlierobservationsby Gäumann (1959). Although pea seedling could be infected by U. viciae-fabae  under controlled conditions, pea accessions werelittle infected under  󿬁 eld conditions by isolates from Australia, theNetherlands, Spain or Syria (Barilli et al., 2009a). Little is known of pathogenicity on pea by other rusts species. U. pisi  is macroscopically identical to  U. viciae-fabae  in the ure-dial stage (being urediospores responsible fordisease developmentunder  󿬁 eld conditions causing a multi-cycling infection), but theycan be distinguished by the morphology of telia and infectionstructures (Emeran et al., 2005; Sillero et al., 2006) as well as by molecular tools (Emeran et al., 2008; Barilli et al., 2011). It seems that  U. pisi  is less specialised than other  Uromyces  species(Gäumann,1959;Emeranetal.,2008),butitshostrangehasnotyet been clari 󿬁 ed. Knowledge about host range of a biotrophic fungus(as  Uromyces ) is of high agronomic and epidemiologic importance.In fact, one of the constraints showed by the species belonging tothis genus is that several rust species may infect the same hostplants ex.  U. viciae-fabae  and  U. pisi  on pea (Barilli et al., 2009b). Inaddition, it is possible that a rust fungus may infect a plant speciesthat previously was thought to be resistant ex.  Medicago  spp. thatwas recently added to  Uromyces ciceris-arietini  host range(Stuteville et al., 2010). These features impede a clear pathogencharacterisation and, as consequence, its control.The purpose of the research reported herewere (i) to determinethe host status of pea against other major legume rusts, (ii) to *  Corresponding author. Tel.:  þ 34 957499211; fax:  þ 34 957499252. E-mail addresses:  ebarilli@ias.csic.es, e.nora@libero.it (E. Barilli). Contents lists available at SciVerse ScienceDirect Crop Protection journal homepage: www.elsevier.com/locate/cropro 0261-2194/$  e  see front matter    2012 Elsevier Ltd. All rights reserved.doi:10.1016/j.cropro.2012.01.019 Crop Protection 37 (2012) 65 e 70  Author's personal copy further de 󿬁 ne the host range of   U. pisi  and (iii) to compare thevirulence of   U. pisi  isolates with different geographical srcin. 2. Materials and methods  2.1. Experiment 1: studying susceptibility of pea to different Uromyces spp. 2.1.1. Fungal isolates and pea accessions Three monopustular isolates of   U. pisi  from different geographicareas and a monopustular isolate each of   Uromyces anthyllidis (Grev.) Schröt.,  U. ciceris-arietini  Jacz. in Boyer & Jacz.,  Uromycesstriatus  J. Schröt.,  U. viciae-fabae  (Pers.) J. Schröt. ex  Vicia faba , U. viciae-fabae  (Pers.) J. Schröt. ex  Vicia sativa  and  Uromyces vignae Barclay (Table 1) were used in the experiment. Isolates weremultiplied on highly susceptible cultivars of their different hosts:pea ( P. sativum  cv. Messire), fenugreek ( Trigonella foenum-graecum L. landrace from Tunisia), chickpea ( Cicer arietinum  L. cv. Fardón),barrel medic ( Medicago truncatula  Gaertn. cv. Baraka), faba bean ( V. faba  L. cv. Baraca), common vetch ( V. sativa  L. cv. Mezquita) andcowpea ( Vigna unguiculata  (L.) Walp. landrace from Egypt).Accessions (listed in Table 2) of   Pisum sativum  ssp.  abysinicum , P. sativum ssp. arvense , P. sativum ssp. elatius , P. sativum ssp.  jornadii , P. sativum  ssp.  sativum ,  P. sativum  ssp.  syriacum ,  P. sativum  ssp. thebaicum , and  P. fulvum  were used in the study.  2.1.2. Host plant propagation and inoculation Toensureexperimentswithauniformplantdevelopmentstage,seeds were germinated during 48 h on wet  󿬁 lter paper in a Petridishat4  C.ThePetridisheswherethentransferredto20  Cduring5 e 7 days. Germinated seeds were planted into plastic pots(6  6  10 cm) 󿬁 lled with a 1:1 mixture of sand and peat in a rust-free growth chamber. There were three consecutive replicationsper fungal isolate, arranged in a complete randomized design. Eachreplicate consisted of 3 pots, each pot containing between 3 and 5plants of each accession depending on their availability. Pea cv.Messire was included in each replication as a susceptible check.Inoculation was done on three-week-old plants, by dusting theplantswith Uromyces  urediospores(2 mgsporesplant  1 )dilutedinpure talc (1:10, w:w) using a spore settling tower. Plants wereincubated for 24 h at 20   C in complete darkness and 100% relativehumidity, then transferred to a growth chamber at 20   C, undera photoperiod of 14/10 h day/night regime, with 148  m mol m  2 s  1 irradiance at plant canopy, as previously mentioned. Every exper-imental set of plants per isolate was maintained apart from theothers in distinct growth chambers.  2.1.3. Disease evaluation and statistical analysis Infection type (IT), and the disease severity (DS) wereobserved 15 days after inoculation, when sporulation occurredprofusely in the susceptible plants. IT was assessed using the 0 e 4scale of  Stackman et al. (1962), where IT 0  ¼  no symptoms,IT ; ¼ necrotic  󿬂 ecks, IT 1 ¼ minute pustules barely sporulating, IT2  ¼  necrotic halo surrounding small pustules, IT 3  ¼  chlorotichalo and IT 4 ¼ well-formed pustules with no associated chlorosisand necrosis. DS was visually estimated as the percentage of symptomatic area of the whole plant, this is, including bothpercentage of pustules and percentage of chlorotic or necrotictissue.For statistical analysis, DS values were angular transformed(180/ p    arcsine [ O (%/100)]) and combined from the three exper-iments to determine average ratings. Comparisons of DS valuesamong accessions of the same species and between differentisolates were subjected to an ANOVA and mean values wereseparated by LSD test at  P   <  0.01. Statistical analyses were per-formed using Statistix (version 8.0; Analytical Software, Talla-hassee, USA).  2.2. Experiment 2: determining the U. pisi host range 2.2.1. Fungal isolates and legume accessions Seven monopustular isolates of   U. pisi  from differentgeographic areas were used in the study (Table 1). Spores werepreserved in liquid nitrogen and multiplied on pea cv. Messirebefore use. Pea plants were grown in pots (6 by 6 by 10 cm)  󿬁 lledwith a 1:1 mixture of sand and peat. When their third or fourthleaves were fully expanded, inoculation was carried out bydusting the plants with rust urediospores. Plants were incubatedfor 24 h at 20   C in complete darkness and 100% relativehumidity, and then transferred to a growth chamber at 20   Cunder a photoperiod at 14 h light and 10 h dark with lightintensity of 148  m mol m  2 s  1 irradiance. After two weeks,urediospores were recollected by means of a vacuum sporecollection device, dried during 24 h in Silica Gel supplied byMerck (Darmstadt, Germany) and stored in refrigerators at  80   Cuntil required for the experiment. Prior to each experiment,urediospores were removed from storage and heat shocked at40   C for 5 min. Each isolate was multiplied apart from the othersto avoid contaminations.Accessions of alfalfa ( Medicago sativa  L.), barrel medic( M. truncatula ), blister vetch ( Vicia ervilia  (L.) Willd.), chickpea ( C.arietinum and Cicer reticulatum L.),chicklingpea( Lathyruscicera L.),common vetch ( V. sativa ), cowpea ( V. unguiculata ), faba bean ( V. faba ), lentil ( Lens culinaris  Medik.), narbon bean ( Vicia narbonensis L.), one 󿬂 ower vetch ( Vicia articulata  Hornem.) and pea ( P. sativum )were used in the study. From 2 to 6 different accessions per specieswere tested (Table 3). Pea cv. Messire was used as susceptiblecontrol in each experiment. Seeds were kindly provided from CGN,Wageningen,Holland(CGN-numbers)andUSDA,WashingtonStateUniversity, USA (PI-numbers).  2.2.2. Host plant propagation and inoculation To ensure experiment with a uniform plant developmentstage, seeds were germinated during 48 h on wet  󿬁 lter paper ina Petri dish at 4   C, as described in experiment 1. Seeds of   V.ervilia ,  V. narbonensis  and  V. unguiculata  were previously scari 󿬁 edby nicking with a razor blade. Replications, experimental designand inoculation were described in experiment 1.  2.2.3. Disease evaluation and statistical analysis Infections type (IT) and the disease severity (DS) were observedas described above. For statistical analysis, data were treated as  Table 1 Codes of reference, geographical srcin and specie of the  Uromyces  isolates used ingrowth chamber experiments at Cordoba (Spain).FungalcodeSpecie Plant specie Collecting siteUaT-01  UromycesanthyllidisT. foenum-graecum  Beja, TunisiaUcaC-01  U. ciceris-arietini C. arietinum  Cuenca, SpainUpCo-01  U. pisi P. sativum  Córdoba, SpainUpKeS-05  U. pisi P. sativum  Kafr-El-Sheik, EgyptUpMo-05  U. pisi P. sativum  Morocco, unknown locationUpPt-03  U. pisi P. sativum  Palmar de Troya, SpainUpRa-05  U. pisi P. sativum  Rabat, MoroccoUpWi-02  U. pisi P. sativum  Winnipeg, CanadaUpZe-04  U. pisi P. sativum   Zidenice, Czech RepublicUsC-01  U. striatus M. sativa  Córdoba, SpainUvfCo-01  U. viciae-fabae V. faba  Córdoba, SpainUvsCo-02  U. viciae-fabae V. sativa  Córdoba, SpainUvC-01  U. vignae V. unguiculata  Canada, unknown location E. Barilli et al. / Crop Protection 37 (2012) 65 e 70 66  Author's personal copy explained in experiment 1, using Statistix (version 8.0; AnalyticalSoftware, Tallahassee, USA). 3. Results  3.1. Experiment 1 All  Pisum  accessions studied displayed a compatible interactionto the three isolates of   U. pisi  tested (Table 2) but DS values rangedfrom 0 to 45%. Accessions belonging to  P. sativum  ssp.  arvense  andssp.  thebaicum were the most susceptible to  U. pisi  isolate UpCo-01,displaying higher DS values ( > 32%).  Pisum fulvum  accessions alsodisplayed compatible IT but very low DS ( < 7%) with the exceptionof P651. Likewise,  U. pisi  isolates UpWi-02 and UpPt-03 induceda compatible response in the whole collection, with DS valuesranging from 3 to 46%.  P. sativum  ssp.  thebaicum  and ssp.  abyssini-cum  were respectively the most susceptible to each isolate(Table 2). Considering the whole  Pisum  collection, no signi 󿬁 cantdifferences were found between  U. pisi  isolates, which showedsimilar infection values. U. anthyllidis  isolate UaT-01 caused low infection types (IT ; and2)andreduceddiseaseseverityvalues(DS < 5%)inmostaccessionsstudied, causing susceptible reaction in some accessions of  P. sativum  ssp.  abyssinicum  and ssp.  elatius  (Table 2). Differencesbetween subspecies were not signi 󿬁 cant ( P  ¼ 0.382).Infectioncausedby U. ciceris-arietini (UcaC-01) wassigni 󿬁 cantlyreduced compared to those achieved by pea, faba bean and vetchrusts ( P  < 0.05), with 3 accessions being either immune (IT 0) (P27,  Table 2 Macroscopic response of a  Pisum  spp. collection against inoculation with different  Uromyces  isolates under controlled conditions. Infection type (IT) and % of disease severity(DS) are reported. Data followed with different small letters, per column and  Pisum  subspecies, are signi 󿬁 cantly different (LSD  P  < 0.01). Data followed with different capitalletters compared, per column, averages between  Pisum  subspecies (LSD  P  < 0.01).Code Species Subsp. UpCo-01 UpWi-02 UpPt-03 UaT-01 UcaC-01 UsC-01 UvfCo-01 UvsCo-02 UvC-01IT a DS b IT DS IT DS IT DS IT DS IT DS IT DS IT DS IT DSP1  P. sativum abyssinicum  4 30ab 4 6.7b 4 32.5ab ; e  2 5.0b 4 0.5a 4 26.0bc 4 6.3bc 4 12.0a 4 1.9aP2  P. sativum abyssinicum  4 34.2a 4 46.0a 4 31.0ab 4 15.0a 4 0.5a 4 41.0a 4 17.0a 4 10.0a 3 0.6aP7  P. sativum abyssinicum  4 20.2b 4 11.7b 4 34.0a 4 4.4b 4 3.2a 4 33.0ab 4 20.0a 4 7.0a 4 0.3aP9  P. sativum abyssinicum  4 39.2a 4 41.7a 4 24.0b 2 0.9b 4 0.1a 4 22.0bc 4 4.2c 4 12.0a 4 0.5aP10  P. sativum abyssinicum  4 22.5b 4 10.0b 4 35.0a 2 0.6b 4 4.6a 4 16.3c 4 12.5ab 4 6.3a 0aAverage 29.2AB 23.2A 31.3A 5.2A 1.7A 27.7A 11.9A 9.5A 0.7AP13  P. sativum elatius  4 28.3a 4 18.0b 4 27.5a 4 41.0a 4 0.8a 4 17.5a 4 41.0a 4 4.2c 4 1.8aP14  P. sativum elatius  e e  4 26.0a 4 38.8a ; 1a ; 1.0c 4 38.8a 4 10.0b 4 0.6aP18  P. sativum elatius  4 22.5ab 4 15.0b 4 26.3a 4 3.7b  e e  4 3.7b ; 3.0c 4 0.3aP19  P. sativum elatius  4 12.1b 4 28.0a 4 25.0a 4 9.0b 4 0.2b 4 9.0b 4 9.0b 4 18.0a 4 0.6aP20  P. sativum elatius  e  4 5.0c 4 25.0a ; 2.3b  e  ; 5.2bc ; 2.3b ; 2.3c 0aAverage 20.9AB 16.5A 25.9AB 18.9A 0.4A 5.1B 18.9A 7.5A 0.6AP26  P. sativum sativum  4 16.7b 4 30.0a 4 26.6a ; 1.6a 4 0.1a 4 21.7a 4 13.3ab 4 0.5b 0bP27  P. sativum sativum  4 28.0ab  e e  ; 4.2a 0a  e e  ; 3.7a 4 0.5abP28  P. sativum sativum  4 45a 4 23.3a 4 25.0a 4 2.6a 4 0.5a 2 12.5a 4 3.6b 0b 3 0.1bP30  P. sativum sativum  4 19.2b 4 27.0a 4 33.0a  e  4 2.7a 4 22.0a 4 18.0a ; 5.0a 4 0.7aP31  P. sativum sativum  e e e  ; 1.0a  e e  4 10.0ab  e  4 0.5abAverage 27.2AB 26.8A 28.2AB 2.4A 0.8A 18.7AB 11.2A 2.3A 0.4AP41  P. sativum arvense  e  4 26.0b  e e e e e e e P42  P. sativum arvense  4 36.0a  e e e e e e e e P316  P. sativum arvense  4 32.5a 4 40.0a 4 22.0a ; e  3 4.0a 4 1.8a 4 10.0a 4 3.4a 2 7.0a 4 0.4aP626  P. sativum arvense  4 40.0a 4 28.0b 4 25.0a ; 0.4b ; 0.4a 4 11.3a 4 10.0a 2 3.4a 4 0.7aP627  P. sativum arvense  e  4 21.7b 4 23.0a ; 0.4b 4 0.4a ; 5.3a 4 6.7a 2 5.0a 4 0.4aAverage 36.3A 28.9A 23.3AB 1.6A 0.9A 8.8B 6.7A 5.1A 0.5AP617  P. sativum thebaicum  4 34.2 4 31.7 4 37.0 ; 2.6 4 0.5 ; 23.0 4 7.0 4 1.6 3 0.5Average 34.2A 31.7A 37.0A 2.6A 0.5A 23.0AB 7.0A 1.6A 0.5AP311  P. sativum syriacum  4 14.2a 4 12.0b 4 26.3a ; 1.3a 0b 4 17.5a 4 0.8b 4 7.5a 0bP665  P. sativum syriacum  4 12.0a 4 35.0a 4 34.0a ; e  2 0.5a 4 5a 4 15.0a 4 28.0a 4 6.3a 4 0.9aAverage 13.1BC 23.5A 30.1AB 0.9A 2.5A 16.2AB 14.4A 6.9A 0.5AP51  P. sativum jornadii  e e e e e e e e e P621  P. sativum jornadii  4 25.8a 4 31.3a 4 13.8a ; 2.5a 4 7.0a ;  e 2 16.7a 4 19.0a ; 7.0a 4 0.4aP649  P. sativum jornadii  4 6.7a 4 8.3b 4 20.0a ; e  2 3.7a 4 5.5a ;  e 2 17.5a  e  ; 3.7b 4 0.1aP650  P. sativum jornadii  4 18.7a 4 23.3ab 4 26.7a  e  4 2.6a 2 16.0a 4 5.3b ; 13.3a 4 0.5aAverage 17.1BC 20.9A 20.1AB 3.1A 5.0A 16.7AB 12.2A 8.0A 0.3AP651  P. fulvum  4 22.5a 4 17.5a  e e  0b ; 4.0a 4 8.0ab 4 23.0a 4 0.5aP658  P. fulvum  4 2.6b 4 23.0a 4 20.0a  e  4 0.3ab ; 2.0a 4 13.7a 4 2.3b 4 0.5aP660  P. fulvum  0 0b 4 6.2b 4 3.0b ; e  2 1.0a ; 0.9a ;  e 2 3.0a 4 7.0ab ; 0.8a 3 0.5aP661  P. fulvum  4 1b 4 22.0a 4 16.4a  e  ; 0.5ab ;  e 2 5.0a 4 17.8a 4 3.7b  e P663  P. fulvum  4 7b 4 18.0a 4 21.3a 4  e  ; 0.4a 4 0.1b 4 1.0a 4 4.2b 4 24.0a 3 0.4aAverage 6.6C 17.3A 15.2B 0.7A 0.4A 3.0B 10.1A 10.8A 0.5ALSD 0.009 0.792 0.0085 0.382 0.239 0.003 0.967 0.401 0.997 e  Non determined. a IT: Infection type following Stackman et al. (1962) scale. b DS:  󿬁 nal disease severity (%) measured under controlled conditions. E. Barilli et al. / Crop Protection 37 (2012) 65 e 70  67
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