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
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.
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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