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First Report of Phyllactinia Chubutiana, Nom. Cons. on Vallesia Glabra (Apocynaceae) in Mexico

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First Report of Phyllactinia Chubutiana, Nom. Cons. on Vallesia Glabra (Apocynaceae) in Mexico Botany First report of Phyllactinia chubutiana, nom. cons. on Vallesia glabra (Apocynaceae) in Mexico Journal: Botany Manuscript ID cjb-2020-0211.R1 Manuscript Type: Note Date Submitted by the 11-Dec-2020 Author: Complete List of Authors: Félix-Gastélum, Rubén; Universidad de Occidente Leyva-Madrigal, Karla ; Universidad de Occidente Quiroz-Figueroa, Francisco ; Instituto Politécnico Nacional Rodriguez-Mora, Norma; Instituto Politécnico Nacional Maldonado-Mendoza,Draft Ignacio ; Instituto Politécnico Nacional Espinosa-Matías, Silvia; Universidad Nacional Autónoma de México Mora-Romero, Guadalupe; Universidad de Occidente, Keyword: Powdery mildew, pearl berry, phylogeny, ITS Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : © The Author(s) or their Institution(s) Page 1 of 24 Botany First report of Phyllactinia chubutiana, nom. cons. on Vallesia glabra (Apocynaceae) in Mexico Rubén Félix-Gastélum1*, Karla Yeriana Leyva-Madrigal1*, Francisco Roberto Quiroz- Figueroa2, Norma Rodriguez-Mora2, Ignacio Eduardo Maldonado-Mendoza2, Silvia Espinosa-Matías3, Guadalupe Arlene Mora-Romero1. 1 Universidad Autónoma de Occidente, Unidad Regional Los Mochis, 81223, Los Mochis, Sinaloa, México. 2 Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR)- Unidad Sinaloa, 81101 Guasave, Sinaloa, México. 3Universidad Nacional Autónoma de México, Facultad de Ciencias, Coyoacán, México, D.F. México CP 04510 Draft *These authors contributed equally to this work. Guadalupe Arlene Mora-Romero, Unidad de Investigación en Ambiente y Salud-Unidad Regional Los Mochis, 81223, Los Mochis, Sinaloa, México, +52 6688161050, fax +52 6688161001, [email protected] Competing interests: The authors declare that there are no competing interests. 1 © The Author(s) or their Institution(s) Botany Page 2 of 24 Abstract A new record of the powdery mildew Phyllactinia chubutiana, nom. cons. (= Oidium insolitum, Ovulariopsis insolita) was documented on pearl berry (Vallesia glabra). No teleomorph was observed. This novel record was identified as a member of Ovulariopsis based on the morphological characteristics of the anamorph (hyphae, conidiophores and conidia), and its hemi-endophytic mycelium in V. glabra correspond to P. chubutiana, nom. cons. A Phyllactinia-specific primer pair was designed for the ITS region of the nuclear rDNA. Phylogenetic analyses confirmed the identity of the powdery mildew specimens found in V. glabra in Sinaloa, Mexico. This is the first ever report of this powdery mildew in V. glabra, and the second report world-wide on a member of the Apocynaceae. Draft Key words: Powdery mildew, pearl berry, phylogeny, ITS. 2 © The Author(s) or their Institution(s) Page 3 of 24 Botany Introduction Powdery mildews adversely affect a range of agricultural and ornamental plants, and the causal agents are biotrophic, obligate parasites (Bushnell 2002). Powdery mildew (PM) fungi disseminate via conidia which are favored by high humidity, but not by rain or immersion in water (Sivapalan 1993a; 1993b). They are members of the family Erysiphaceae in the order Helotiales, and parasitize around 9,838 angiosperm species (Amano 1986); 93% of host plants are dicotyledons, while 7% are monocotyledons (Takamatsu 2013). The mycelium of PM fungi is usually epiphytic, except in the genera Leveillula, Phyllactinia, Pleochaeta, and in one species of Cystotheca in which the mycelium is hemi- endophytic. In the latter case, the pathogen produces superficial hyphae that penetrate the leaves through the stomata and produceDraft mycelia inside, in contrast to Leveillula species where mycelia are abundant within the leaf of the host plant (Braun et al. 2002). The current knowledge regarding PM in Sinaloa, Mexico is in its early stages. Reported examples include Podosphaera xanthii (Castagne) U. Braun and Shishkoff in cucurbits and husk tomatoes (Physalis philadelphica Lam.), Pseudoidium anacardii (F. Noack) U. Braun and R. T. A. Cook on mango, Erysiphe diffusa (Cooke and Peck) U. Braun and S. Takam. on common bean, and Podosphaera pannosa (Wallr.) de Bary on roses (Félix- Gastélum et al. 2016). In addition, Golovinomyces spadiceus (Berk. and M.A. Curtis) U. Braun was reported in wild sunflower (Félix-Gastélum et al. 2019). In recent years, Phyllactinia (Ovulariopsis cf. insolita) was reported on Funastrum clausum (Jacq.) Schltr. and F. cynanchoides (Decne.) Schltr. (Bojórquez-Ramos et al. 2014). Vallesia glabra (Cav.) Link (Apocynaceae) is a perennial shrub that grows in tropical and subtropical areas of the Americas (Castañeda-Montoya 2018), including 22 of the 32 Mexican states (Juárez-Jaimes et al. 2007). We observed signs of PM on the leaves of this 3 © The Author(s) or their Institution(s) Botany Page 4 of 24 species in the municipalities of Navolato, Guasave, Ahome and El Fuerte in Sinaloa, Mexico, from February through April, 2020. During sampling collection, we observed that PM was most severe in the lower part of the canopy, mainly in shaded plants growing under perennial trees such as poplar (Populus dimorpha T. S. Brandeg), Manila tamarind (Pithecellobium dulce (Roxb.) Benth), and flame tree (Delonix regia (Bojer ex Hook.) Raf). The initial signs of the disease consist of small white patches (0.5-1.5 mm in diameter), but as the disease progresses it covers the total abaxial surface of the leaf (Figures 2B and 2C). No signs of the pathogen were observed on the adaxial surface of the leaves. Abundant structures of the anamorph of the pathogen were observed on infected leaves, however the teleomorph was not observed during the sampling period. Preliminary microscopy observations of the asexualDraft structures of the powdery mildew indicated that the fungus associated with the PM disease belongs to the genus Ovulariopsis, an anamorph of the genus Phyllactinia (Havrylenko et al. 2006; Bojórquez-Ramos et al. 2014). Seven hundred species of deciduous trees belonging to 69 families distributed mainly in the temperate regions of the northern hemisphere have been found to be affected by PM, in which species of Phyllactinia have been implicated as the causal agent of PM (Amano 1986). In Argentina, P. chubutiana Harvryl, Takam. and U. Braun (the teleomorph of O. insolita (U. Braun, Kiehr and Delhey) Havryl, S. Takam. and U. Braun) was reported on Lycium chilense Miers ex Bertero. To identify this fungal species, morphological features of both the teleomorph and the anamorph were examined and molecular techniques were used (Havrylenko et al. 2006; Braun and Cook 2012). Additionally, Phyllactinia (Ovulariopsis cf. insolita) was reported for the first time on F. clausum and F. cynanchoides in Mexico; since 4 © The Author(s) or their Institution(s) Page 5 of 24 Botany the teleomorph of the fungus was not observed, the identification included morphological features of the anamorph and molecular techniques (Bojórquez-Ramos et al. 2014). The objective of the present study was to identify the fungus associated with PM on V. glabra in Mexico. To the best of our knowledge, there are no other reports on the incidence of PM disease on this host plant in Mexico, or anywhere else in the world. Materials and methods Sample collection Ten samples of V. glabra leaves with signs of PM were collected from February 10 through April 15, 2020 in the coastal regionsDraft of the Ahome, El Fuerte, Guasave and Navolato municipalities in Sinaloa, Mexico from 7 to 15 masl (Table 1). There was no rain during the sampling periods, and the average temperature varied from 13 to 29°C. Samples were placed in an ice chest at 8-10°C and taken to the laboratory and processed within 48 h after collection. A representative symptomatic sample was deposited at the herbarium of the Universidad Autónoma de Occidente in Los Mochis, Sinaloa, Mexico. Light microscopy and scanning electron microscopy of asexual structures Specimens were collected from the abaxial leaf surfaces of samples to be used in the morphometric studies. Slide mounts of mycelia, conidiophores and conidia were prepared by touching the whitish lesions with clear adhesive tape, and then placing the tape in a drop of lactophenol-cotton-blue dye on a microscope slide, followed by measuring at 400X magnification with the aid of an ocular and stage micrometer in a compound microscope (Labomed; Labo America, Inc., USA). The hyphal width, distance of septum from the 5 © The Author(s) or their Institution(s) Botany Page 6 of 24 branching point of the conidiophore, foot cell length, conidiophore length and width at its midpoint, and the length and width of mature conidia (detached from the conidiophore) were all measured. Forty structures of the anamorph from ten sampling sites (Table 1) were measured (n=400). Images of the structures were obtained using a compound microscope (Axio Imager M2; Carl Zeiss, Gottingen, Germany) with the same procedure as for the measurements. Micrographs of conidia were taken with a JEOL JSM-53110 LV scanning electron microscope (Bozzola and Russel 1999), after fixing the samples as described by Ruzin (1999). Microscopic analysis of infected leaves Dry infected leaf samples (ca. 0.5 cm) were fixed in 50% ethanol for 24 h at room temperature. Fixed samples were dehydratedDraft through an ethanol series (50, 70, 85, and 100%) for 2 h in each solution. Subsequently, the leaf fragments were transferred to xylol-ethanol (1:1) for 1 h, 100% xylol for 1 h, and finally embedded in paraffin at 55-60°C during 3 h. The infiltrated
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