The anamorphic state of Leveillula taurica was found causing a powdery mildew disease on Cleome spinosa in north-eastern Brazil. Its chasmothecial state was not observed on the collected samples. The fungus is illustrated and described. This report represents the first record of this fungus on Cleome spinosa in Brazil

Carlos AC

Soares DJ

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Mycosphere Doi 10.5943/mycosphere/3/3/3 289 The anamorphic state of Leveillula taurica recorded on Cleome spinosa in north-eastern Brazil    Carlos AC1 and Soares DJ2*  1Universidade Estadual da Paraíba, Rua Baraúnas, 351 - Bairro Universitário - Campina Grande/PB, CEP 58429-500 2Embrapa Algodão, Ruas Oswaldo Cruz 1143 – Bairro Centenário - Campina Grande/PB, Brazil, CEP 58428-095  Carlos  AC, Soares DJ 2012 – The  anamorphic  state of Leveillula taurica recorded on Cleome spinosa in north-eastern Brazil. Mycosphere 3(3), 289–292, Doi 10.5943 /mycosphere/3/3/3  The  anamorphic  state  of  Leveillula  taurica  was  found  causing  a  powdery  mildew  disease  on Cleome spinosa in north-eastern Brazil. Its chasmothecial state was not observed on the collected samples. The  fungus  is  illustrated and described. This report represents the  first record of this fungus on Cleome spinosa in Brazil.  Key words – Erysiphales – Oidiopsis – powdery mildew – spiny spiderflower  Article Information  Received 30 March 2012 Accepted 2 April 2012 Published online 11 May 2012 *Corresponding author: Dartanha J. Soares – e-mail – dartjs@yahoo.com.br  Introduction The  genus  Cleome  L.  belongs  to Cleomaceae (Capparaceae s.l.) and has appro-ximately  250  species;  most  are  adapted  to seasonal drought. Several species are used as medicinal  or  ornamental,  while  a  few  are regarded as weeds (Mabberley 2008). Cleome spinosa  Jacq.,  popularly  known  as  spiny spider-flower  could  be  included  in  the  last category. In semiarid regions of north-eastern Brazil,  where  drought  is  quite  frequent,  this plant  is  widespread,  but  occurs  mainly  near humid lowlands (Lorenzi 2000).  In December of 2010 scattered plants of C.  spinosa  whit  a  white  powdery  mass covering  its  leaves  where  observed  in  the experimental  field  of  the  Embrapa  Algodão (Brazilian  Center  of  Cotton  Research)  in Paraíba  State.  A  sample  was  collected  and examined  under  a  microscope  revealing  the presence  of  a  fungus  that  was  identified  as belonging  to  the  genus  Oidiopsis  Scalia,  the anamorphic  state  of  Leveillula  G.  Arnaud. After that, during field trips in 2011 and 2012 plants of C. spinosa showing the same white powdery  mass  were  observed  in  several  new locations through Paraíba State. New samples were  collected  and  after  a  microscopic examination a fungus with similar morphology of that previously identified as Oidiopsis was observed.  There  are  several  erysiphaceous fungi recorded on the genus Cleome, but only two  belonging  to  Leveillula,  viz.  L.  taurica (Lév.) G. Arnaud (Farr & Rossman 2012) and L.  cleomes  Simonyan  &  V.P.  Heluta (Simonyan  &  Heluta  1989).  The  aim  of  this study  was  describe  the  morphology  and identify  the  species  of  the  powdery  mildew fungus occurring on C. spinosa in north-eastern Brazil.  Methods  Examined samples   Leaves of Cleome spinosa covered with a white powdery mass were collected from the municipalities of Campina Grande (December 2010,  January  2012),  Juazeirinho  (December 2011) and Pombal (December 2011) in Paraíba State, north-eastern Brazil. The samples were Mycosphere Doi 10.5943/mycosphere/3/3/3 290   Fig. 1 – Map of Brazil with Paraíba State enlarged showing the three localities where samples were collected. A Campina Grande. B Juazeirinho. C Pombal. (Images from Google Maps®)  dried in a plant press and later examined under a stereomicroscope. Representative material of each of the examined samples was deposited in the Herbarium of the ‘Universidade Federal de Viçosa’ (Herbarium VIC).  Morphological studies To identify the powdery mildew fungus microscope slides were prepared by free-hand section,  scraping  the  colonies  with  a  scalpel, and also by using an adhesive tape. Lactic acid, lacto-fuchsin and water were used as mounting media.  The  microscope  slides  were  prepared from  fresh  and  dried  specimens  and  gently warmed.  Measurements  were  made  at  a magnification  of  1000  X  using  an  Olympus microscope.   Results Five  samples,  three  from  Campina Grande (VIC 31815; VIC 31816; VIC 31819), one  from  Juazeirinho  (VIC  31818)  and  one from Pombal (VIC 31817), all in Paraíba State, in north-eastern Brazil (Fig. 1), were collected showing  similar  symptoms  (Fig.  2).  The disease is characterized by amphigenous white powdery colonies, initially as small circular to irregular  colonies,  becoming  somewhat  vein-delimited and later usually covering the entire leaf  blade,  mainly  on  the  lower  surface. Mycelium hemi-endophytic; internal mycelium tortuous, ca 2–5 µm diam.,  hyaline, reaching the palisade parenchyma and  bearing globose to  mulberry-like  haustoria;  superficial  myce-lium  hyaline,  5–7.5  µm  diam.,  flexuous, bearing  branched  coral-like  appressoria; conidiophores  originate  from  the  internal mycelium,  emerging  singly  or  in  bundles through  the  stomata;  straight  to  slightly flexuous,  usually  ramified,  mostly  with  1-septum near the base and 2–3-septa at the distal end, 5–7 µm diam. near the base, up to 300 µm long,  hyaline;  conidia  dimorphic;  primary conidia lanceolate, hyaline, (51–)60–68(–75) × (11–)13–15.5 µm, l/w ratio 3.5–5.4; secondary conidia  subcylindrical  to  slightly  clavate, hyaline,  (41–)50–60(–68)  ×  (11–)13–15(–17) µm,  l/w  ratio  2.9–5.8,  apex  usually  rounded, base  somewhat  truncate;  germination,  on natural substrata, usually at basal end with or without appressoria formation (Fig. 2).  Discussion Two Leveillula species are known from Cleome  spinosa  (viz.  L.  taurica  and  L. cleomes)  Based  in  the  morphological  and biometric  description  the  fungus  collected  in north-eastern  Brazil  was  identified  as  the anamorphic  stage  of  Leveillula  taurica  [= Oidiopsis  haplophylii  (H.  Magn.)  Rulamort]. The main distinctions between our specimens and  L.  cleomes  are  the  slender  conidia  and bigger  l/w  ratio.  L.  cleomes  has  primary  and secondary conidia varying from 48–79 × 14–21 µm and 51–70 × 13–21 µm, with l/w ratio 2.6–4.5  and  2.7–4.8,  respectively.  Our  samples have  somewhat  narrower  primary  and secondary conidia varying from 51–79 × 11–15.5 µm and 41–68 × 11–17 µm, with a larger l/w ratio of 3.5–5.4 and 2.9–5.8, respectively. On  the  other  hand,  L.  taurica  has  conidia varying from 30–80 × 12–22 µm, with l/w ratio Mycosphere Doi 10.5943/mycosphere/3/3/3 291   Fig.  2  –  Leveillula  taurica  on  Cleome  spinosa.  a,  b,  c  Symptoms  on  leaves.  d  Conidia  and conidiophores. e Detail of a conidiophore arising through a stoma. f Primary conidium. g, h, i Secondary conidia. j Conidiophore with a young conidium. k, l Branched, coral-like appressoria. m Mulberry-like  haustorium.  n  A  primary  conidium  germinating  at  base  without  appressorium formation – Bars = 10 µm, except in d = 100 µm.  2.5–4.5 (Braun 1987). Additionally L. taurica is a polyphagous pathogen occurring on more than  100  genera  of  host  plants,  with  a worldwide  distribution  while  L.  cleomes  is known  only  from  the  type  collection  from Armenia  (Simonyan  &  Heluta  1989).  L. taurica  has  been  recorded  on  C.  spinosa  in Europe  and  Africa  (Farr  &  Rossman  2012), and also on C. hassleriana in North America (Sampangi  et  al.  2007).  Several  papers  have been  published  recently  on  the  taxonomic status  of  species  within  the  genus  Leveillula, especially  L.  taurica,  using  molecular  tools (Khodaparast  et  al.  2001,  2002,  2007,  2011) and  some  new  species  have  been  segregated from L. taurica s.l. However, its taxonomical status  remains  controversial.  In  view  of  this, and the fact that the size of the conidia of L. Mycosphere Doi 10.5943/mycosphere/3/3/3 292 taurica on different host plants as well as on a single host is extremely variable (Braun 1980), we  decided  to  adopt  a  conservative  point  of view about our specimens. This record represents the first report of L. taurica on C. spinosa in Brazil and also for the American continent. Cleome spinosa has no commercial  interest  in  Brazil,  but  is  usually regarded  a  weed;  this  host  has  a  wide distribution throughout the country and it may be  a  reservoir  of  this  pathogen  for  a  diverse range of crops.  Acknowledgements The senior author would like to thank Paul  Kirk, Joost Stalpers and Vincent Robert for their help in obtaining the cited literature.  References  Braun  U.  1980  –  The  genus  Leveillula  –  a preliminary study. Nova Hedwigia 32, 565–583. Braun  U.  1987  –  A  Monograph  of  the Erysiphales  (Powdery  Mildews).  J. Cramer, Berlin-Stuttgart.  Farr  DF,  Rossman  AY.  2012  –  Fungal Databases,  Systematic  Mycology  and Microbiology  Laboratory,  ARS, USDA. Retrieved 12 March 2012, from http://nt.ars-grin.gov/fungaldatabases/ Khodaparast  SA,  Takamatsu  S,  Hedjaroude GA.  2001  –  Phylogenetic  structure  of the  genus  Leveillula  (Erysiphales: Erysiphaceae)  inferred  from  the nucleotide sequences of the rDNA ITS region with special reference to the L. taurica  species  complex.  Mycological Research, 105, 909–918. Khodaparast SA, Hedjaroude GA, Takamatsu S, Braun U. 2002 – Three new species of  the  genus  Leveillula  from  Iran. Mycoscience 43, 459–462. Khodaparast  SA,  Niinomi  S,  Takamatsu  S. 2007  –  Molecular  and  morphological characterization  of  Leveillula (Ascomycota:  Erysiphales)  on monocotyledonous plants. Mycological Research, 111: 673–679. Khodaparast  SA,  Takamatsu  S,  Harada  M, Abbasi M, Samadi S. 2011 – Additional rDNA  ITS  sequences  and  its phylogenetic  consequences  for  the genus  Leveillula  with  emphasis  on conidium  morphology.  Mycological Progress  doi  10.1007/s11557-011-0785-7 Lorenzi H. 2000 – Plantas Daninhas do Brasil. Instituto Plantarum, Nova Odessa. Mabberley  DJ.  2008  –  Mabberley’s  Plant-Book: A portable dictionary of plants, their classification and uses. Cambridge University Press, Cambridge. Sampangi R, Glawe DA, Mohan SK. 2007 – First  North  American  record  of powdery mildew of Cleome hassleriana caused  by  Leveillula  taurica.  Online. Plant  Health  Progress, doi:10.1094/PHP-2007-0219-02-BR.  Simonyan SA, Heluta VP. 1989 – New species of powdery mildew fungus of the genus Leveillula Arnaud on the spiderflower. Biologicheskii  Zhurnal  Armenii  42, 480–482.       

mycosphere

The anamorphic state of Leveillula taurica recorded on Cleome spinosa in north-eastern Brazil

CARLOS, A. C.

SOARES, D. J.

Repository Open Access to Scientific Information from Embrapa

Mycosphere Doi 10.5943/mycosphere/3/3/3 289 The anamorphic state of Leveillula taurica recorded on Cleome spinosa in north-eastern Brazil    Carlos AC1 and Soares DJ2*  1Universidade Estadual da Paraíba, Rua Baraúnas, 351 - Bairro Universitário - Campina Grande/PB, CEP 58429-500 2Embrapa Algodão, Ruas Oswaldo Cruz 1143 – Bairro Centenário - Campina Grande/PB, Brazil, CEP 58428-095  Carlos AC, Soares DJ 2012 – The anamorphic state of Leveillula taurica recorded on Cleome spinosa in north-eastern Brazil. Mycosphere 3(3), 289–292, Doi 10.5943 /mycosphere/3/3/3  The anamorphic state of Leveillula taurica was found causing a powdery mildew disease on Cleome spinosa in north-eastern Brazil. Its chasmothecial state was not observed on the collected samples. The fungus is illustrated and described. This report represents the first record of this fungus on Cleome spinosa in Brazil.  Key words – Erysiphales – Oidiopsis – powdery mildew – spiny spiderflower  Article Information  Received 30 March 2012 Accepted 2 April 2012 Published online 11 May 2012 *Corresponding author: Dartanha J. Soares – e-mail – dartjs@yahoo.com.br  Introduction The genus Cleome L. belongs to Cleomaceae (Capparaceae s.l.) and has appro-ximately 250 species; most are adapted to seasonal drought. Several species are used as medicinal or ornamental, while a few are regarded as weeds (Mabberley 2008). Cleome spinosa Jacq., popularly known as spiny spider-flower could be included in the last category. In semiarid regions of north-eastern Brazil, where drought is quite frequent, this plant is widespread, but occurs mainly near humid lowlands (Lorenzi 2000).  In December of 2010 scattered plants of C. spinosa whit a white powdery mass covering its leaves where observed in the experimental field of the Embrapa Algodão (Brazilian Center of Cotton Research) in Paraíba State. A sample was collected and examined under a microscope revealing the presence of a fungus that was identified as belonging to the genus Oidiopsis Scalia, the anamorphic state of Leveillula G. Arnaud. After that, during field trips in 2011 and 2012 plants of C. spinosa showing the same white powdery mass were observed in several new locations through Paraíba State. New samples were collected and after a microscopic examination a fungus with similar morphology of that previously identified as Oidiopsis was observed. There are several erysiphaceous fungi recorded on the genus Cleome, but only two belonging to Leveillula, viz. L. taurica (Lév.) G. Arnaud (Farr & Rossman 2012) and L. cleomes Simonyan & V.P. Heluta (Simonyan & Heluta 1989). The aim of this study was describe the morphology and identify the species of the powdery mildew fungus occurring on C. spinosa in north-eastern Brazil.  Methods  Examined samples  Leaves of Cleome spinosa covered with a white powdery mass were collected from the municipalities of Campina Grande (December 2010, January 2012), Juazeirinho (December 2011) and Pombal (December 2011) in Paraíba State, north-eastern Brazil. The samples were Mycosphere Doi 10.5943/mycosphere/3/3/3 290   Fig. 1 – Map of Brazil with Paraíba State enlarged showing the three localities where samples were collected. A Campina Grande. B Juazeirinho. C Pombal. (Images from Google Maps®)  dried in a plant press and later examined under a stereomicroscope. Representative material of each of the examined samples was deposited in the Herbarium of the ‘Universidade Federal de Viçosa’ (Herbarium VIC).  Morphological studies To identify the powdery mildew fungus microscope slides were prepared by free-hand section, scraping the colonies with a scalpel, and also by using an adhesive tape. Lactic acid, lacto-fuchsin and water were used as mounting media. The microscope slides were prepared from fresh and dried specimens and gently warmed. Measurements were made at a magnification of 1000 X using an Olympus microscope.   Results Five samples, three from Campina Grande (VIC 31815; VIC 31816; VIC 31819), one from Juazeirinho (VIC 31818) and one from Pombal (VIC 31817), all in Paraíba State, in north-eastern Brazil (Fig. 1), were collected showing similar symptoms (Fig. 2). The disease is characterized by amphigenous white powdery colonies, initially as small circular to irregular colonies, becoming somewhat vein-delimited and later usually covering the entire leaf blade, mainly on the lower surface. Mycelium hemi-endophytic; internal mycelium tortuous, ca 2–5 µm diam., hyaline, reaching the palisade parenchyma and bearing globose to mulberry-like haustoria; superficial myce-lium hyaline, 5–7.5 µm diam., flexuous, bearing branched coral-like appressoria; conidiophores originate from the internal mycelium, emerging singly or in bundles through the stomata; straight to slightly flexuous, usually ramified, mostly with 1-septum near the base and 2–3-septa at the distal end, 5–7 µm diam. near the base, up to 300 µm long, hyaline; conidia dimorphic; primary conidia lanceolate, hyaline, (51–)60–68(–75) × (11–)13–15.5 µm, l/w ratio 3.5–5.4; secondary conidia subcylindrical to slightly clavate, hyaline, (41–)50–60(–68) × (11–)13–15(–17) µm, l/w ratio 2.9–5.8, apex usually rounded, base somewhat truncate; germination, on natural substrata, usually at basal end with or without appressoria formation (Fig. 2).  Discussion Two Leveillula species are known from Cleome spinosa (viz. L. taurica and L. cleomes) Based in the morphological and biometric description the fungus collected in north-eastern Brazil was identified as the anamorphic stage of Leveillula taurica [= Oidiopsis haplophylii (H. Magn.) Rulamort]. The main distinctions between our specimens and L. cleomes are the slender conidia and bigger l/w ratio. L. cleomes has primary and secondary conidia varying from 48–79 × 14–21 µm and 51–70 × 13–21 µm, with l/w ratio 2.6–4.5 and 2.7–4.8, respectively. Our samples have somewhat narrower primary and secondary conidia varying from 51–79 × 11–15.5 µm and 41–68 × 11–17 µm, with a larger l/w ratio of 3.5–5.4 and 2.9–5.8, respectively. On the other hand, L. taurica has conidia varying from 30–80 × 12–22 µm, with l/w ratio Mycosphere Doi 10.5943/mycosphere/3/3/3 291   Fig. 2 – Leveillula taurica on Cleome spinosa. a, b, c Symptoms on leaves. d Conidia and conidiophores. e Detail of a conidiophore arising through a stoma. f Primary conidium. g, h, i Secondary conidia. j Conidiophore with a young conidium. k, l Branched, coral-like appressoria. m Mulberry-like haustorium. n A primary conidium germinating at base without appressorium formation – Bars = 10 µm, except in d = 100 µm.  2.5–4.5 (Braun 1987). Additionally L. taurica is a polyphagous pathogen occurring on more than 100 genera of host plants, with a worldwide distribution while L. cleomes is known only from the type collection from Armenia (Simonyan & Heluta 1989). L. taurica has been recorded on C. spinosa in Europe and Africa (Farr & Rossman 2012), and also on C. hassleriana in North America (Sampangi et al. 2007). Several papers have been published recently on the taxonomic status of species within the genus Leveillula, especially L. taurica, using molecular tools (Khodaparast et al. 2001, 2002, 2007, 2011) and some new species have been segregated from L. taurica s.l. However, its taxonomical status remains controversial. In view of this, and the fact that the size of the conidia of L. Mycosphere Doi 10.5943/mycosphere/3/3/3 292 taurica on different host plants as well as on a single host is extremely variable (Braun 1980), we decided to adopt a conservative point of view about our specimens. This record represents the first report of L. taurica on C. spinosa in Brazil and also for the American continent. Cleome spinosa has no commercial interest in Brazil, but is usually regarded a weed; this host has a wide distribution throughout the country and it may be a reservoir of this pathogen for a diverse range of crops.  Acknowledgements The senior author would like to thank Paul Kirk, Joost Stalpers and Vincent Robert for their help in obtaining the cited literature.  References  Braun U. 1980 – The genus Leveillula – a preliminary study. Nova Hedwigia 32, 565–583. Braun U. 1987 – A Monograph of the Erysiphales (Powdery Mildews). J. Cramer, Berlin-Stuttgart.  Farr DF, Rossman AY. 2012 – Fungal Databases, Systematic Mycology and Microbiology Laboratory, ARS, USDA. Retrieved 12 March 2012, from http://nt.ars-grin.gov/fungaldatabases/ Khodaparast SA, Takamatsu S, Hedjaroude GA. 2001 – Phylogenetic structure of the genus Leveillula (Erysiphales: Erysiphaceae) inferred from the nucleotide sequences of the rDNA ITS region with special reference to the L. taurica species complex. Mycological Research, 105, 909–918. Khodaparast SA, Hedjaroude GA, Takamatsu S, Braun U. 2002 – Three new species of the genus Leveillula from Iran. Mycoscience 43, 459–462. Khodaparast SA, Niinomi S, Takamatsu S. 2007 – Molecular and morphological characterization of Leveillula (Ascomycota: Erysiphales) on monocotyledonous plants. Mycological Research, 111: 673–679. Khodaparast SA, Takamatsu S, Harada M, Abbasi M, Samadi S. 2011 – Additional rDNA ITS sequences and its phylogenetic consequences for the genus Leveillula with emphasis on conidium morphology. Mycological Progress doi 10.1007/s11557-011-0785-7 Lorenzi H. 2000 – Plantas Daninhas do Brasil. Instituto Plantarum, Nova Odessa. Mabberley DJ. 2008 – Mabberley’s Plant-Book: A portable dictionary of plants, their classification and uses. Cambridge University Press, Cambridge. Sampangi R, Glawe DA, Mohan SK. 2007 – First North American record of powdery mildew of Cleome hassleriana caused by Leveillula taurica. Online. Plant Health Progress, doi:10.1094/PHP-2007-0219-02-BR.  Simonyan SA, Heluta VP. 1989 – New species of powdery mildew fungus of the genus Leveillula Arnaud on the spiderflower. Biologicheskii Zhurnal Armenii 42, 480–482.       

The anamorphic state of Leveillula taurica recorded on Cleome spinosa in north-eastern Brazil

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