Pathogenic Microorganisms Infecting Berries in Mexico

 

Edith Garay-Serrano1,2*, Samuel Cruz-Esteban1,2, Sylvia P. Fernández Pavia3, Gerardo Rodríguez Alvarado3 and Nuria Gómez-Dorantes3

1Instituto de Ecología, A.C. Red de Diversidad Biológica del Occidente Mexicano. Avenida Lázaro Cárdenas 253, 61600 Pátzcuaro, Michoacán, México

2CONACYT. Avenida Insurgentes Sur 1582, 03940 Ciudad de México, México

3Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Unidad Posta Zootecnica, Carretera Morelia, Zinapécuaro km 9.5, C.P. 58880, Tarímbaro, Michoacán, México

*For correspondence: edith.garay@inecol.mx

Received 04 September 2020; Accepted 25 January 2021; Published 16 April 2021

 

Abstract

 

Mexico is one of the major producers of berries worldwide and ranks third amongst the principal exporters of these fruits. However, the presence of diseases in crops of blueberry, blackberry, strawberry, and raspberry in production areas of the country, has a negative impact in production yields. In this work, we presented a revision of all pathogens reported for these berries during the last 64 years in Mexico. Data on the different groups of pathogens including bacteria, stramenopila, and fungi, as well as location and references, are listed for the several types of berries produced. The pathogen species names were actualized according to the current taxonomic status following the specialized nomenclatural websites. Perspectives for future research are discussed. © 2021 Friends Science Publishers

 

Keywords: Blackberry; Blueberry; Oomycota; Phytopathogenic bacteria; Raspberry; Strawberry

 


Introduction

 

Berries are becoming some of the favorite fruits in many countries. During 2018, the total global production of berries was 6.16 million ton (FAOSTAT 2020). The United States, Mexico and Poland accounted for 54% of the total production worldwide in 2018. Mexico was the world's leading producer of blackberries (Rubus ulmifolius) with 287,125 tons, second producer of raspberries (Rubus idaeus) with 130,187 tons, the second in strawberry (Fragaria x ananassa) production with 653,639 tons, and the fifth producer of blueberries (Vaccinium corymbosum) with 40,251 tons (FAOSTAT 2020).

In Mexico, berries are produced all year round using irrigated and non-irrigated systems (SIAP 2018; SADER-SIAP 2019). Among the 23 states that cultivate berries (Fig. 1), the highest production comes from the states of Baja California, Jalisco and Michoacan (SIAP 2018). This last, is the main producer of blackberries (96% of national production) and strawberries (70%), while Jalisco is the principal producer of blueberries (46%) and raspberry (71%) (SIAP 2018).

Berry crops are attacked by a large number of plant pathogens including bacteria, fungi and oomycetes. These microorganisms induce diseases in most of the plant organs such as leaves, stems, inflorescences, fruits, and roots, reducing crop yields during pre- and postharvest. Several species are becoming a problem in berries worldwide, some as the bacteria Xanthomonas fragariae in strawberry (Kastelein et al. 2014; Kamangar et al. 2017; Wang et al. 2017), the oomycete Phytophthora cinnamomi inducing crown and root rot in V. corymbosum (Tamietti 2003; Larach et al. 2009; Huarhua et al. 2018), the fungi Fusarium oxysporum causing wilt disease in blackberry (Gordon et al. 2016; Pastrana et al. 2017) and blueberries (Liu et al. 2014; Moya-Elizondo et al. 2019), or several species of Lasiodiplodia in different berries, as Lasiodiplodia theobromae causing dieback in strawberry

 

Fig. 1: Percentage of cultivated berries´s production volume for each state in Mexico

 

(Nam et al. 2016) or inducing stem blight and dieback of blueberry plants (Wright and Harmon 2009; Scarlett et al. 2019; Rodríguez-Gálvez et al. 2020).

Recently in Mexico, Neofusicoccum algeriense was detected in berries causing dieback in raspberry for the first time (Serret-López et al. 2017). In addition, Neopestalotiopsis rosae was reported inducing root rot, crown rot and leaf spot in strawberry in Central Mexico, causing losses of up to 50% of transplanted plants (Rebollar-Alviter et al. 2020). N. rosae is a new pathogen of strawberry that should be considered as an emerging threat to this fruit crop (Rebollar-Alviter et al. 2020).

The objective of the study was to compile all the references of diseases caused by bacteria, fungi and oomycetes, on commercial crops and wild berries in Mexico. This work includes those reports where plant pathogens were identified using molecular and/or morphological techniques, and the studies were published in scientific papers, books or databases. We consider that this work will be useful for plant pathologists, plant breeders and other scientists that work with berries in Mexico and elsewhere.

 

Materials and Methods

 

We conducted a fully comprehensive search on databases of scientific articles, books, and conference proceedings containing reports of diseases of berries, including blackberry, blueberry, raspberry and strawberry, from Mexico during the last 64 years. Our interest was to focus on reports where molecular and/or morphological analyses were utilized to identify the pathogens affecting these crops. Additionally, a search was conducted in the National Fungus Collections of The Agricultural Research Service of the US Department of Agriculture (Farr and Rossman 2019).

The information collected was organized in a database that included hosts, locality, affected tissue of the plant, the name of the induced disease and the bibliographic reference. Subsequently, the information was ordered according to its taxonomic classification by kingdom, phylum, family, scientific name, and author of the species. The scientific names of the pathogens were corroborated using List of Prokaryotic names with Standing in Nomenclature (LPSN) (Parte et al. 2020; www.bacterio.net/-classifphyla.html.), Index Fungorum website (www.indexfungorum.org), and MycoBank Database (http://www.mycobank.org/).

The taxonomic names of the berry plants were verified using GBIF Secretariat (2019), also the distribution of berry plants reported was accessed to know if these plants have restricted or wide distribution in González-Elizondo and González-Elizondo (2014), and Rzedowski and Calderón (2005).

 

Results

 

Diseases of berries were reported in 17/32 states of Mexico. A total of the pathogens reported affecting berries crops in Mexico is listed in Table 1.

 

Pathogenic microorganisms by crop

 

A total of 319 records of plant pathogens causing diseases on berries from Mexico during the period of 1956 to 2020, were detected in the accessed databases. These reports included diseases caused by bacteria, fungi, and oomycetes. The records included 54 genus of plant pathogens represented by 88 species. Five species corresponded to bacteria (5.7%), 75 corresponded to fungi (85.2%), and eight were oomycetes (9.1%). Bacteria belong to 3 families, Stramenopila species appertain to 1 phylum (oomycota) and 2 families, and the fungi representing the largest pathogens group affecting berries, they are grouped in three phyla and 27 families.

Strawberry was the crop most affected with 53 pathogens, raspberry and blackberry presented 29 and 26 pathogens, respectively, while for blueberry there were only 16 pathogens reported (Table 2).

The genera of pathogen most reported were Agrobacterium, Alternaria, Botrytis, Colletotrichum, Fusarium, Gerwasia, Phytophthora, Podosphaera, Rhizoctonia and Verticillium. While the most frequently reported species were Agrobacterium radiobacter, Fusarium oxysporum, Gerwasia rubi, and Kuehneola loeseneriana affecting Rubus species; Botrytis cinerea, Peronospora sparsa in blackberry; Alternaria spp., Botrytis cinerea, Colletotrichum spp., Fusarium oxysporum, Ramularia grevilleana, Rhizoctonia solani, Verticillium albo-atrum and V. dahlia in strawberry; and Colletotrichum spp. and Thekopsora minima in blueberry.

 

Botanical host species

 

Most of the reports of berries diseases in Mexico were referred in cultivated species such as Vaccinium corymbosum (blueberry), Rubus idaeus (raspberry), Rubus ulmifolius (blackberry), and Fragaria x ananassa, a hybrid of strawberry. However, different botanical host species were also reported being affected by phytopathogens: the wild blackberries Rubus adenotrichos and Rubus humistratus, or the wild strawberry Fragaria mexicana and other species reported in Table 3 where the distributions are shown.

Table 1: Phytopathogenic bacteria, oomycete and fungi inducing berries diseases reported in Mexico, arranged hierarchically by taxonomic group. Synonyms indicated in parentheses

 

PHYLLUM

FAMILY

PATHOGEN

DISEASE

HOST

LOCALITY

REFERENCE

BACTERIA

 

 

 

 

 

 

Proteobacteria

Lysobacteraceae

Xanthomonas fragariae

Angular leaf spot

Strawberry

Guanajuato, Michoacán, Morelos

García-Álvarez 1976; Narro-Sánchez et al. 2006; Fernández-Pavía et al. 2014

 

Rhizobiaceae

Agrobacterium radiobacter

(=Agrobacterium tumefaciens)

Crown and cane gall

Raspberry, strawberry, blackberry

Baja California, Ciudad de México, Estado de México, Michoacán

García-Álvarez 1976, 1981, Fernández-Pavía et al. 2015, López-Aranda et al. 2016

Tenericutes

Acholeplasmataceae

Candidatus Phytoplasma spp. group 16SrXIII-(A/I)I

Green petal, periwinkle virescence, inedible fruit

Blueberry, raspberry, strawberry, blackberry

Jalisco, Michoacán

Pérez-López and Dumonceaux 2016, Pérez-López et al. 2017

 

 

Candidatus Phytoplasma spp. group Aster yellow

Green petal, periwinkle plants with virescence

Strawberry

Guanajuato, Michoacán

Narro-Sánchez et al. 2006

 

 

Candidatus Phytoplasma spp. group 16SrXIII

Green petal, periwinkle plants with virescence

Strawberry

Michoacán

Avendaño-Benequen et al. 2017

STRAMENOPILA

 

 

 

 

 

 

Oomycota

Peronosporaceae

Peronospora sparsa

Downy mildew (dryberry)

Blackberry

Michoacán, México, does not specify locality

Tejera and Ochoa 2004; Agustín and García 2007; Horst 2013; Rodríguez-Díaz et al. 2017

 

 

Phytophthora cactorum

Leather rot on fruit and crown rot and wilt

Strawberry

Estado de México, Guanajuato, Michoacán

Castro-Franco et al. 1993; Mendoza-Zamora and Romero-Cova 1989; Narro-Sánchez et al. 2006; Fernández-Pavía et al. 2015

 

 

Phytophthora capsici

Fruit rot

Strawberry

Estado de México

Mendoza-Zamora and Romero-Cova 1989

 

 

Phytophthora fragariae var. fragariae

Red stele root rot

Strawberry

Michoacán

Ceja-Torres et al. 2008

 

 

Phytophthora rubi (=Phytophthora fragariae var. rubi)

Root rot

Raspberry

México, does not specify locality

López-Aranda et al. 2016

 

 

Phytophthora spp.

Root rot and dry wilt

Strawberry

Estado de México, Guanajuato, Michoacán

García-Álvarez 1976; Castro-Franco and Dávalos 1990; Mendoza 1992; Fraire-Cordero et al. 2003; Ceja-Torres et al. 2008, Fernández-Pavía et al. 2015

 

Pythiaceae

Pythium aphanidermatum

Dry wilt

Strawberry

Michoacán

Ceja-Torres et al. 2008

 

 

Pythium spp.

Dry wilt

Raspberry

Jalisco

López-Aranda et al. 2016

FUNGI

 

 

 

 

 

 

Ascomycota

Aspergillaceae

Aspergillus spp.

Soft fruit rot

Strawberry

Michoacán

Fraire-Cordero et al. 2003

 

 

Penicillium spp.

Soft fruit rot

Strawberry

Michoacán

Fraire-Cordero et al. 2003

 

Botryosphaeriaceae

Lasiodiplodia spp.

Necrosis of leaves, branches and stems

Blackberry

Michoacán

Contreras-Pérez et al. 2019

 

 

Neofusicoccum algeriense

Dieback

Raspberry

Michoacán

Serret-López et al. 2017

 

 

Neofusicoccum parvum

Stem Blight and Dieback

Blueberry, blackberry

Jalisco, Michoacán

Boyzo-Marin et al. 2016

 

 

Neofusicoccum spp.

Stem canker

Blueberry

Michoacán

Mondragón-Flores et al. 2012

 

 

Sphaeropsis spp.

Fruit rot

Strawberry

Estado de México, Guanajuato

García-Álvarez 1976

 

Chaetomiaceae

Chaetomium spp.

Plant bud blight

Blueberry

Michoacán

Mondragón-Flores et al. 2012

 

Cladosporiaceae

Cladosporium spp.

Blossom blight

Strawberry

México, Michoacán

Fraire-Cordero et al. 2003

 

Diaporthaceae

Phomopsis obscurans (=Dendrophoma obscurans)

Leaf blight

Strawberry

Estado de México

Mendoza-Zamora and Romero-Cova 1988

 

 

Phomopsis spp.

Stem canker

Blueberry

Michoacán

Mondragón-Flores et al. 2012

 

Didymellaceae

Ascochyta spp.

Marginal leaf spot or leaf blight

Strawberry

Estado de México, Guanajuato

Mendoza-Zamora and Romero-Cova 1988

 

 

Phoma spp.

Stem canker, root and crown rot

Blueberry, strawberry

Estado de México, Guanajuato, Michoacán

Mendoza-Zamora and Romero-Cova 1989; Mondragón-Flores et al. 2012

 

Dipodascaceae

Geotrichum spp.

Soft fruit rot

Strawberry

Michoacán

Fraire-Cordero et al. 2003

 

Drepanopezizaceae

Diplocarpon earlianum (=Diplocarpon earliana)

Leaf scorch

Strawberry

Estado de México, Guanajuato, Morelos

García-Álvarez 1976; Narro-Sánchez et al. 2006; Fernández-Pavía et al. 2015

 

 

Diplocarpon fragariae (=Marssonina fragariae)

Leaf scorch

Strawberry

Estado de México

Mendoza-Zamora and Romero-Cova 1988

 

 

Marssonina spp. (=Gloeosporium spp.)

Leaf scorch

Strawberry

Aguascalientes, Estado de México, Hidalgo, Michoacán

García-Álvarez 1981; Mendoza-Zamora and Romero-Cova 1988; Fernández-Pavía et al. 2015

 

Elsinoaceae

Elsinoe veneta

Cane spot

Raspberry, blackberry

Puebla, México, does not specify locality

García-Álvarez 1976

 

Erysiphaceae

Podosphaera aphanis (=Sphaerotheca macularis f. fragariae)

Powdery mildew

Strawberry

Estado de México, Guanajuato, Michoacán

García-Álvarez 1976; Mendoza-Zamora and Romero-Cova 1988; Narro-Sánchez et al. 2006

Table 1: Continued

 


Table 1: Continued

 

 

 

Podosphaera macularis (=Sphaerotheca humuli)

Powdery mildew

Strawberry

Chihuahua, Guanajuato, Jalisco, Morelos

García-Álvarez 1976; Fernández-Pavía et al. 2015

 

 

Podosphaera spp.

Powdery mildew

Blackberry

Michoacán

Tejera & Ochoa 2004; Agustín and García 2007

 

Glomerellaceae

Colletotrichum acutatum

Anthracnose fruit rot

Strawberry

Michoacán

Espinoza-Altamirano et al. 2017

 

 

Colletotrichum gloeosporioides

Anthracnose

Blackberry

México, does not specify locality

Horst 2013

 

 

Colletotrichum spp.

Anthracnose fruit rot, leaf blight

Blueberry, raspberry, strawberry

Estado de México, Guanajuato, Jalisco, Michoacán, Morelos

García-Álvarez 1976; Fraire-Cordero et al. 2003; Narro-Sánchez et al. 2006; Ceja-Torres et al. 2008; Mondragón-Flores et al. 2012; Fernández-Pavía et al. 2015; López-Aranda et al. 2016

 

Meliolaceae

Appendiculella calostroma

Sooty mold

Blackberry

Veracruz

Farr and Rossman 2019

 

Mycosphaerellaceae

Cercospora spp.

Leaf Spot

Raspberry, strawberry

Jalisco, México, does not specify locality

García- Álvarez 1981; Fernández-Pavía et al. 2015; López-Aranda et al. 2016

 

 

Cercosporella spp.

Rosette

Raspberry, blackberry

Ciudad de México

García- Álvarez 1981

 

 

Mycosphaerella rubi (=Septoria rubi)

Leaf spot

Raspberry, blackberry

Puebla, México, does not specify locality

García- Álvarez 1976, 1981; Farr and Rossman 2019

 

 

Ramularia grevilleana (=Ramularia tulasnei, Mycosphaerella fragariae)

Leaf spot

Strawberry

Estado de México, Guanajuato, Michoacán, México, does not specify locality

García- Álvarez 1976, 1981; Mendoza-Zamora and Romero-Cova 1988; Narro-Sánchez et al. 2006; Fernández-Pavía et al. 2015; Farr and Rossman 2019

 

 

Septoria darrowii

Leaf spot

Blackberry

México, does not specify locality

Farr and Rossman 2019

 

 

Septoria spp.

Leaf spot

Raspberry, blackberry

Ciudad de México

García- Álvarez 1976

 

Nectriaceae

Albonectria rigidiuscula (=Fusarium rigidiusculum)

Root and crown rot

Strawberry

Estado de México

Mendoza-Zamora and Romero-Cova 1989

 

 

Cylindrocarpon spp.

Black Root Rot

Strawberry

Guanajuato, Michoacán

Ceja-Torres et al. 2008; Mariscal-Amaro et al. 2017

 

 

Fusarium brachygibbosum

Dry wilt

Strawberry

Guanajuato

Mariscal-Amaro et al. 2017

 

 

Fusarium equiseti

Dry wilt

Raspberry

Jalisco

López-Aranda et al. 2016

 

 

Fusarium fujikuroi

(=Fusarium subglutinans, F. verticillioides, F. moniliforme)

Dry wilt

Raspberry, strawberry

Jalisco, Guanajuato, Michoacán

Mendoza-Zamora and Romero-Cova 1989; López-Aranda et al. 2016; Mariscal-Amaro et al. 2017

 

 

Fusarium oxysporum

Dry wilt

Blackberry, raspberry, strawberry

Estado de México, Guanajuato, Jalisco, Michoacán, Morelos

Téliz-Ortíz et al. 1986; Mendoza-Zamora and Romero-Cova 1989; Castro-Franco and Dávalos 1990; Ceja-Torres et al. 2008; Gordon et al. 2016; López-Aranda et al. 2016; Mariscal-Amaro et al. 2017; Bárcenas-Santana et al. 2019

 

 

Fusarium oxysporum

Dry wilt

Blackberry, raspberry, strawberry

Estado de México, Guanajuato, Jalisco, Michoacán, Morelos

Téliz-Ortíz et al. 1986; Mendoza-Zamora and Romero-Cova 1989; Castro-Franco and Dávalos 1990; Ceja-Torres et al. 2008; Gordon et al. 2016; López-Aranda et al. 2016; Mariscal-Amaro et al. 2017; Bárcenas-Santana et al. 2019

 

 

Fusarium oxysporum f. spp. mori

Dry wilt

Blackberry

Michoacan, México, does not specify locality

Pastrana et al. 2017; Hernández-Cruz et al. 2020

 

 

Fusarium oxysporum f. spp. fragariae

Fusarium wilt of strawberry

Strawberry

Guanajuato, Michoacán

Dávalos-González et al. 2004; Narro-Sánchez et al. 2006

 

 

Fusarium proliferatum

Vascular Wilt

Strawberry

Guanajuato

Mariscal-Amaro et al. 2017

 

 

Fusarium pseudonygamai

Dry wilt

Strawberry

Guanajuato

Mariscal-Amaro et al. 2017

 

 

Fusarium roseum

Dry wilt

Strawberry

Estado de México

Mendoza-Zamora and Romero-Cova 1989

 

 

Fusarium spp.

Dry wilt

Raspberry, strawberry, blackberry

Ciudad de México, Estado de México, Guanajuato, Michoacán, México, does not specify locality

García-Álvarez 1976, 1981; Mendoza-Zamora and Romero-Cova 1989; Castro-Franco and Dávalos 1990; Mendoza 1992; Dávalos-González et al. 2004; Fernández-Pavía et al. 2015

Table 1: Continued

 

Table 1: Continued

 

 

 

Neocosmospora solani (=Fusarium solani)

Crown and root rot

Raspberry, strawberry

Estado de México, Guanajuato, Jalisco, Michoacán

Mendoza-Zamora and Romero-Cova 1989; Ceja-Torres et al. 2008; López-Aranda et al. 2016; Mariscal-Amaro et al. 2017

 

Pestalotiopsidaceae

Neopestalotiopsis rosae

Crown and root rot

Strawberry

Michoacán

Rebollar-Alviter et al. 2020

 

 

Pestalotiopsis spp.

Crown and root rot

Blueberry, strawberry

Michoacán, Puebla

Fraire-Cordero et al. 2003; Mondragón-Flores et al. 2012; Morales-Mora et al. 2019

 

Phyllostictaceae

Phyllosticta spp.

Phyllosticta leaf spot

Blueberry, strawberry

Baja California, Estado de México, Michoacán,

García-Álvarez 1976; Mendoza-Zamora and Romero-Cova 1988; Mondragón-Flores et al. 2012

 

Plectosphaerellaceae

Verticillium albo-atrum

Verticillium wilt

Raspberry, strawberry

Guanajuato, Jalisco, Michoacán, México, does not specify locality.

García-Álvarez 1976, 1981; Ceja-Torres et al. 2008; Fernández-Pavía et al. 2015; López-Aranda et al. 2016

 

 

Verticillium dahliae

Verticillium wilt

Strawberry

Estado de México, Guanajuato, Michoacán

Téliz-Ortíz et al. 1986; Castro-Franco and Dávalos 1990; Mendoza 1992;

 

 

Verticillium spp.

Verticillium wilt

Raspberry, strawberry

Guanajuato, Michoacán, México, does not specify locality

Narro-Sánchez et al. 2006; López-Aranda et al. 2016

 

Pleosporaceae

Alternaria alternata

Leaf Spot

Strawberry

Guanajuato

Mariscal-Amaro et al. 2017

 

 

Alternaria spp.

Leaf spot, dry wilt, soft fruit rot, root rot

Blueberry, raspberry, strawberry, blackberry

Aguascalientes, Baja California, Durango, Estado de México, Guanajuato, Jalisco, Michoacán, Oaxaca

García-Álvarez 1976, 1981; Fraire-Cordero et al. 2003; Narro-Sánchez et al. 2006; Mondragón et al. 2012; Fernández-Pavía et al. 2015; López-Aranda et al. 2016

 

 

Bipolaris spp.

Blueberry blight

Blueberry

Michoacán

Mondragón et al. 2012

 

 

Curvularia spp.

Stem scab

Blueberry

Michoacán

Mondragón et al. 2012

 

 

Stemphylium spp.

Silver stain

Blueberry

Michoacán

Mondragón et al. 2012

 

Sclerotiniaceae

Botrytis cinerea

Gray mold, Botrytis blossom blight

Strawberry, blackberry

Colima, Estado de México, Guanajuato, Jalisco, México, does not specify locality, Michoacán, Morelos

García-Álvarez 1976, 1981; Mendoza-Zamora and Romero-Cova 1988; Tejera and Ochoa 2004; Narro-Sánchez et al. 2006; Agustín and García 2007; Fernández-Pavía et al. 2015; Álvarez-Medina et al. 2017

 

 

Botrytis spp.

Gray mold

Strawberry

Michoacán

Fraire-Cordero et al. 2003

 

Venturiaceae

Coleroa chaetomium

Leaf spot

Blackberry

Estado de México

Romero-Cova 1990

 

Xylariaceae

Rosellinia spp.

Root rot

Raspberry, blackberry

Durango

García-Álvarez 1976

Basidiomycota

Ceratobasidiaceae

Rhizoctonia fragariae

Root rot

Strawberry

Michoacán

Ceja-Torres et al. 2008

 

 

Rhizoctonia solani

Root rot, fruit rot

Raspberry, strawberry

Estado de México, Guanajuato, Jalisco, México, does not specify locality, Michoacán, Morelos, Nayarit, Sonora

García-Álvarez 1976, 1981; Téliz-Ortíz et al. 1986; Mendoza-Zamora and Romero-Cova 1989; Castro-Franco and Dávalos 1990; Mendoza 1992; López-Aranda et al. 2016

 

 

Rhizoctonia spp.

Root rot

Strawberry

Guanajuato, Michoacán

Narro-Sánchez et al. 2006

 

Phragmidiaceae

Gerwasia pittieriana

Rust

Raspberry, blackberry

Morelos, México, does not specify locality

León-Gallegos and Cummnins 1981

 

 

Gerwasia rubi

Rust

Raspberry, blackberry

Michoacán, Morelos, Veracruz, México, does not specify locality,

López et al. 1980; León-Gallegos and Cummnins 1981; López 1984

 

 

Gymnoconia nitens

Rust

Raspberry, blackberry

Puebla, México, does not specify locality

León-Gallegos and Cummnins 1981

 

 

Kuehneola arthurii

Rust

Blackberry

México, does not specify locality

León-Gallegos and Cummnins 1981

 

 

Kuehneola loeseneriana

Rust

Raspberry, blackberry

Veracruz, México, does not specify locality,

López et al. 1980; León-Gallegos and Cummnins 1981; López 1984; Hernández and Hennen 2003

 

 

Mainsia rubi (=Uromyces rubi)

Rust

Raspberry, blackberry

México, does not specify locality, Puebla, Veracruz

Watson 1971; García-Álvarez 1976; Farr and Rossman 2019

 

 

Phragmidium mexicanum (=Frommea mexicana)

Rust

Strawberry

México, does not specify locality

Cummins and Stevenson 1956; Watson 1971; García-Álvarez 1976; Fernández-Pavía et al. 2015

Table 1: Continued

 

Text Box: Table 1: Continued

		Phragmidium occidentale	Rust	Raspberry	Veracruz	Carrion and Galvan 1987
		Phragmidium spp.	Rust	Raspberry, blackberry	Puebla	García-Álvarez 1981
	Pucciniastraceae	Naohidemyces vaccinii (=Pucciniastrum vaccinii, Naohidemyces vacciniorum)	Late leaf rust	Blueberry	Durango, México, does not specify locality	León-Gallegos and Cummnins 1981
		Pucciniastrum americanum	Leaf rust	Raspberry	Estado de México, Jalisco, Michoacán	Rebollar-Alviter et al. 2001a, b; Marín et al. 2019
		Pucciniastrum spp.	Leaf rust	Blueberry	Michoacán	Mondragón-Flores et al. 2012
		Thekopsora minima	Leaf rust	Blueberry	Jalisco, Michoacán, México, does not specify locality	Rebollar-Alviter et al. 2011; Horst 2013
Mucoromycota	Mucoraceae	Mucor spp.	Soft fruit rot	Strawberry	Michoacán	Fraire-Cordero et al. 2003
	Rhizopodaceae	Rhizopus stolonifer (=Rhizopus nigricans)	Soft fruit rot	Strawberry, blackberry	Estado de México, Guanajuato, México, does not specify locality, Michoacán	García-Álvarez 1976; Fraire-Cordero et al. 2003; Chávez-Díaz et al. 2014; Fernández-Pavía et al. 2015 

Table 2: Species of pathogenic microorganisms reported affecting berries, organized by Kingdom

	Bacteria	Stramenopila	Fungi	Pathogenic species by crop
Blue berry	1	0	15	16
Rasp berry	2	2	25	29
Straw berry	5	5	43	53
Black berry	2	1	23	26
Total pathogenic species by group	5	8	75	88

Table 3: Berry plant species reported to be affected for plant pathogens microorganism in Mexico

Family	Berry 	Scientific name	Characteristics and distribution
Ericaceae	Blueberry	Vaccinium corymbosum L.	Widely cultivated species. E.U. and North Hemisphere*
		Vaccinium geminiflorum Kunth	Mexican blueberry. Dwarf blueberry, Distributed from Alaska to Guatemala**
 	 		
Rosaceae	Raspberry	Rubus idaeus L.	Widely cultivated species. Native of Europe and North Asia*
 	 	Rubus trilobus Moc. & Sessé ex Ser.	Guatemala and southern and central Mexico*
Rosaceae	Strawberry	Fragaria x ananassa (Weston) Duchesne	North America to Patagonia. 
 	 	Fragaria mexicana Schltdl.	Wild Mexican strawberry. Mexico*
Rosaceae	Blackberry	Rubus adenotrichos Schltdl.	Wild blackberry. Distributed from central Mexico to Ecuador. The fruits are highly collected in Michoacan***
 	 	Rubus fruticosus L.	Cultivated species. North and south Hemisphere*
		Rubus humistratus Steud	Wild blackberry. Endemic species of Mexico***
 	 	Rubus ulmifolius Schott	Cultivated species. Europe, North Africa, America and Oceania*
Source: *GBIF Secretariat (2019), ** González-Elizondo and González-Elizondo (2014), *** Rzedowski and Calderón (2005)
Discussion

 

Berries plant protection include several strategies, but one of them is to know the pathogens that potentially affect the crops, especially considering that pest (understood as pathogens, animals, and weed) in global level, could cause annual crop yield losses from 20 to 40% of the production (Oerke 2006; Savary et al. 2012).

In this compilation of phytopathogens affecting berries in Mexico, fungi were the largest group reported with 75 of a total of 88 species of microorganism. The most common fungal pathogens included Botrytis cinerea, Fusarium oxysporum and Colletotrichum spp.; while the bacterium Agrobacterium rhizobacter, and the oomycete Peronospora sparsa and Phytophthora cactorum, were some of the most common pathogens reported. These fungi and bacteria are considered amongst the top plant pathogens due to the severe economic losses that cause worldwide, and their scientific importance (Dean et al. 2012; Mansfield et al. 2012). Other reported pathogens such as Thekopsora minima in blueberry (Rebollar-Alviter et al. 2011), and Rhizoctonia solani in strawberry (Mouden et al. 2016; Amrutha and Vijayaraghavan 2019; Errifi et al. 2019) should also be considered as highly important due to the reductions on yields that cause (Ahmed et al. 2017).

A major deficiency in 35% of the reports that were analyzed was the lack of identification to the species level. More recent studies have included molecular techniques to assess the taxonomic species (Boyzo-Marin et al. 2016; Serret-López et al. 2017; Contreras-Pérez et al. 2019). However, in the cases of Colletotrichum and Fusarium, the presence of species complexes makes difficult to establish the correct identification of the involved species due to the probable presence of cryptic species. To identify species in these species complexes is necessary to use several molecular markers (Pastrana et al. 2017; Hernández-Cruz et al. 2020). The use of multilocus identification may detect new species such as Neopestalotiopsis rosae reported in strawberry (Rebollar-Alviter et al. 2020).

Although pathogens in wild species of berries in Mexico have been scarcely studied, some wild hosts were referenced (Table 3). These plants might be capable of harboring pathogens that could serve as inoculum source reservoirs for the infection of nearby crops (Grünwald et al. 2001; Pak et al. 2017).

The information of phytopathogens affecting berries in Mexico will allow to researchers to detect areas of opportunity to focus on, and for technicians to have a benchmark about all the pathogens in each berry crop that have been reported. Knowing the pathogens will help to plant management strategies to combat infection caused by phytopathogens.

 

Conclusion

 

Records of bacteria, oomycetes and pathogenic fungi reported in berries in Mexico since 1956 to 2020 added up to a total of 88 species. Phytopathogenic bacteria are represented by 5.7% of the species, 9.1% correspond to oomycetes and 85.2% to fungi. Still there are phytopathogenic species that need more in-depth taxonomic studies, coupled with this, there are several lineages integrating species complex that need to delve into molecular, genetic and physiological studies to understand in a better way the strategies to control the field diseases.

 

Acknowledgements

 

EG thanks to Jazmín Cortés Martínez for the support provided in the collection of initial data.

 

Author Contributions

 

EG and SC generated the idea of the study. EG, SC, SPF, and NG collected the data. EG prepared the initial manuscript; performed the tables. SC, SPF, GR analyzed the data to be considered. All authors commented on the manuscript, reviewed drafts of the paper, and approved the final draft.

 

Conflicts of Interest

 

All other authors declare no conflicts of interest

 

Data Availability

 

Not applicable.

 

Ethics Approval

 

Not applicable.

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