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Pathogenesis mechanisms employed by Alternaria species

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Pathogenesis mechanisms employed by Alternaria species

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Alternaria species are mainly saprophytic fungi, but some have acquired pathogenic capacities causing plant diseases over a broad host range. More than 70 phytotoxins are produced by them from which only a small proportion have been chemically characterized and reported to act as mycotoxins. Host-selective toxins (HSTs) produced by Alternaria plant pathogens are generally low-molecular-weight secondary metabolites with a diverse range of structures that function as effectors controlling pathogenicity or virulence in certain plant–pathogen interactions. This review summarizes all the diseases caused by Alternaria spp., mycotoxins produced by Alternaria spp. and the recent advances in elucidating mode of action of host specific Alternaria toxins at physiological, biochemical and molecular levels.
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213Journal of Oilseed Brassica, 6 (2) July., 2015
Pathogenesis mechanisms employed by Alternaria species
Gohar Taj*, PD Meena1, Priyanka Giri, Dinesh Pandey, Arvind Kumar2 and Anil Kumar
Molecular Biology and Genetic Engineering, College of Basic Science and Humanities,
G.B. Pant Univ. of Agriculture & Technology, Pantnagar-263145, US Nagar, Uttarakhand, India
1ICAR-Directorate of Rapeseed-Mustard Research, Bharatpur, 321 303 Rajasthan, India
2RLB Central Agricultural University, Jhansi, 284 003 Uttar Pradesh, India
*Correspondence author: gohartajkhan@rediffmail.com
(Received: 10 February 2015; Revised: 06 June 2015; Accepted: 18 June 2015)
Abstract
Alternaria species are mainly saprophytic fungi, but some have acquired pathogenic capacities causing plant
diseases over a broad host range. More than 70 phytotoxins are produced by them from which only a small
proportion have been chemically characterized and reported to act as mycotoxins. Host-selective toxins
(HSTs) produced by Alternaria plant pathogens are generally low-molecular-weight secondary metabolites
with a diverse range of structures that function as effectors controlling pathogenicity or virulence in certain
plant–pathogen interactions. This review summarizes all the diseases caused by Alternaria spp., mycotoxins
produced by Alternaria spp. and the recent advances in elucidating mode of action of host specific
Alternaria toxins at physiological, biochemical and molecular levels.
Keywords: Alternaria spp., mechanism, mode of action, phytopathogenesis, toxin
Journal of Oilseed Brassica, 6 (2): 213-240, July 2015
Introduction
The genus Alternaria includes many saprophytic
and endophytic species. It was first described by
Nees in 1816 with Alternaria tenuis as the only
species, which was later renamed as Alternaria
alternata (Fr.) Keissl. (Meena et al., 2010). All
Alternaria species lack sexuality, and are thus
classified into (kingdom fungi, sub-kingdom
Eumycotera, phylum fungi Imperfecti, form class
Hypomycetes, form order Moniliales, form family
Dematiaceae, genus Alternaria). Many pathogenic
Alternaria species produce toxins which facilitate
their necrotrophic life style. Prior to colonization,
necrotrophs kill their host cells at a distance by
producing both toxins, and lytic enzymes. They
often trigger genetically- programmed apoptotic
pathways, or directly cause cell damage resulting in
necrosis. Many species of Alternaria produce
toxins with broad host ranges, but some agronomically
important species produce host-specific toxins with
a narrow range often to the cultivar level. Alternaria
species are important pathogen of many crucifers
which also produces carcinogenic, teratogenic and
mutagenic mycotoxins. Researchers around the
globe are using this necrotrophic pathogen to study
molecular mechanisms of plant defense (Oliver &
Ipcho, 2004, Thaler et al., 2004, Rowe &
Kliebenstein, 2010).
Lawrence et al. (2008) used Alternaria brassicicola
(Schwein.) Wiltshire as a model representative for
their basic research on virulence and generalized
the role of toxins in the pathogenesis mechanism
employed by Alternaria genus. Chung (2012) also
studied the stress response and pathogenecity of the
necrotrophic fungal pathogen Alternaria alternata.
This review summarizes the recent advances in
pathogenesis of Alternaria spp. at physiological,
biochemical and molecular levels, and also discusses
the present understanding of the mode of
Alternaria host specific toxins.
Plant diseases caused by Alternaria species
The genus Alternaria includes both non-pathogenic
and pathogenic species causing diseases on
agronomically important plants including cereals,
ornamentals, oilcrops, vegetables and fruits in table
1 (Rahman et al., 2002, Thomma, 2003, Agrios, 2005,
Raja et al., 2006, Meena et al., 2010).
214 Journal of Oilseed Brassica, 6 (2) July., 2015
Table 1. Alternaria species causes various diseases on different hosts
Species Host Symptoms Location Reference
A. acalyphae Kucing Galak Leaf spot Seychelles Kingsland, 1984
(Acalypha indica) Islands
A. alternata Aloe (Aloe vera) Leaf spot Pakistan Bajwa et al., 2010
Aloe (Aloe vera) Leaf spot Louisiana da silva & Singh, 2012
Almond (Prunus dulcis) Leaf spot California Teviotdale et al., 2001
Apple (Malus Communis) Postharvest Decay Pennsylvania Jurick et al., 2014
during Cold Storage
Barbados nut (Jatropha curcas) Inflorescence blight Sinaloa (Mexico) Angeles et al., 2012
Baby’s breath Leaf spot Bulgaria Margina et al., 1999
(Gypsophila paniculata)
Banana (Musa) Leaf spot United States Parkunan et al., 2013
Big leaf hydrangea Leaf spot Italy Garibaldi et al., 2007
(Hydrangea macrophylla)
Big bend bluebonnet Stem blight Texas Colbaugh et al., 2001
(Lupinus havardii)
Desert zinnia (Zinnia acerosa) Flower blight Texas Colbaugh et al., 2001
Bladder dock (Rumex vesicarius) Leaf spot India Sankar et al., 2012
Black mangrove Leaf spot China Lin et al., 2014
(Bruguiera gymnorrhiza)
Cherry (Prunus avium) Leaf spot Greece Thomidis &
Tsipouridis, 2006
Cherry fruits (Prunus avium) Black spot China Zhao & Liu, 2012
Compass plant Blight Poland Wagner &
(Silphium laciniatum) Jamiolkowska, 2004
Cotton (Gossypium hirsutum) Stem canker - Laidou et al., 2000
Chinese dwarf Banana (Musa) Leaf spot China Fu et al., 2014
Crown flower Leaf spot Rajasthan Sain et al., 2009
(Calotropis gigantean)
Cucumber (Cucumis sativus) Leaf spot - Vakalounakis, 1990
Desert Zinnia (Zinnia acerosa) Flower blight Texas Colbaugh et al., 2001
Date Palm (Phoenix dactylifera) Postharvest Spain Palou et al., 2013
Black Spot
English walnut (Juglans regia) Leaf spot - Belisario et al., 1999
Fig (Ficus carica) Fruit Rot Montenegro Latinovic et al., 2014
Gopher plant (Euphorbia lathyris) Blight China Yu et al., 2011
Heart-leaved houttuynia Leaf spot China Zheng et al., 2011
(Houttuynia cordata)
Hop cones (Humulus lupulus) Infection Australia Pethybridge et al., 2001
Kiwifruit (Actinidia deliciosa) Dieback - Tsahouridou &
Thanassoulopoulos, 2000
215Journal of Oilseed Brassica, 6 (2) July., 2015
Kiwifruit (Actinidia deliciosa) Leaf spot Turkey Karakaya & Celik, 2012
Kiwifruit (Actinidia deliciosa) Leaf spot Italy Corazza et al., 1999
Lemon (Citrus) Brown spot Yunnan Wang et al., 2010
Province China
Lime (Citrus) Brown spot Peru Marin et al., 2006
Lemon (Citrus) Black rot - Peever & Carpenter
Boggs, 2005
Lemon (Citrus) Brown Spot Spain Vicent et al., 2000
Marigold (Tagetes erecta) Leaf Spot Beijing, China Li et al., 2014
Melon Leaf spot Mid-Atlantic Zhou & Everts, 2008
Region of the
United States
Pomegranate (Punica Granatum) Black spot Spain Berbegal et al., 2014
Peace lily (Spathiphyllum) Leaf spot Argentina Cheheid et al., 2000
Paneer dodi (Withania coagulans) Leaf Spot India Sharma et al., 2013
Philodendron (Philodendron) Leaf Spot China Zhou et al., 2014
Potatoe (Solanum tuberosum) Leaf Blight South Africa van der Waals et al. 2011
Prickly-ash (Zanthoxylum piperitum) Blight China Yang et al., 2013
Switchgrass (Panicum virgatum) Leaf Spot Tennessee Vu et al., 2012
Tobacco (Nicotiana tabacum) Brown spot Connecticut and LaMondia, 2001
Massachusetts
Tomato (Solanum lycopersicum) Leaf blight Pakistan Akhtar et al., 2004
Toothed Dock (Rumex dentatus) Leaf Spot Pakistan Siddiqui et al., 2009
Thorowax (Bupleurum chinense) Leaf blight China Zhang et al., 2010
Tea (Camellia sinensis) Leaf spot China Zhou & Xu, 2014
Vine spinach (Basella alba) Leaf blight India Sankar et al., 2011
Wonder tree (Idesia polycarpa) Leaf spot China Sun et al., 2014
A. arborescens Tomato (Solanum lycopersicum) Stem canker - Kirk et al., 2008
A. arbusti Asian pear (Pyrus pyrifolia) Leaf lesions - Kirk et al., 2008
A. arotiincultae Carrot (Daucus carota) - New Zealand Trivedi et al., 2010
A. bataticola Sweet potato (Ipomoea batatas) Leaf spot and South America Lopes & Boiteux, 1994
stem blight
A. blumeae Hunchback’s mother Lesions - Kirk et al., 2008
(Blumea aurita)
A. brassicae Daikon (Raphanus sativus Leaf spot California Koike & Molinar, 1997
cv. longipinnatus)
Whitetop (Lepidium draba) Leaf Spot North America Caesar & Lartey, 2009
Canola Gray leaf spot Argentina Gaetan & Madia, 2005
Abyssinian Kale Leaf spot Australia You et al., 2005
(Crambe abyssinicia)
A. brassicicola Cauliflower (Brassica oleracea) Leaf blight Rajasthan Porwal & Kothari, 1970
Field Pannycress (Thlaspi arvense) Leaf spot Geneva, NY Cobb & Dillard, 1998
Dyer’s Woad Leaf (Isatis indigotica) Leaf spot China Gao et al., 2014
216 Journal of Oilseed Brassica, 6 (2) July., 2015
A. brunsii Cumin (Cuminum cyminum) Blossom blight - Kirk et al., 2008
A. cassiae Cowpea (Vigna unguiculata) - - Grange & Aveling, 1998
A. cichorii Radicchio (Cichorium intybus) Leaf spot California Koike & Butler, 1998
A. carthami Snow lotus (Saussurea laniceps) Leaf spot China Zhao et al., 2008
Safflower (Carthamus tinctorius) - - Kirk et al., 2008
Snow Lotus (Saussurea laniceps) Leaf Spot China Zhao et al., 2008
A. carotiincultae Carrot (Daucus carota) Leaf blight - Kirk et al., 2008
A. conjuncta Parsnip (Pastinaca sativa) - - Kirk et al., 2008
A. cucumerina Cucurbit (Cucurbita argyrosperma) - - Kirk et al., 2008
Pumpkin (Cucurbita pepo) Leaf spot North Caucasus Gannibal, 2011;
(Russia) Sikora, 1994
A. cinerariae Leopard plant (Farfugiu japonicum) Leaf spot Japan Sakoda et al., 2010
A. compacta Climbing hydrangea (Hydrangea Leaf spot Italy Garibaldi et al., 2008
anomala subsp. Petiolaris)
A. chlamydospora Ashwagandha (Withania somnifera) Leaf blight - Vanitha, 2008
A. cheiranthi Wallflower (Erysimum cheiri) - - Bambridge et al., 1985
A. dauci Carrot (Daucus carota) Leaf blight Israel Ben-Noon et al., 2001
Carrot (Daucus carota) - - Kirk et al., 2008
A. dianthicola Ashwagandha Leaf blight India Maiti et al., 2007
(Withania somnifera)
A. dichondrae Kidney grass (Dichondra repens) Leaf blight Australia Sivapalan & Pascoe,
1994
A. euphorbiicola Cole - - Kirk et al., 2008
A. gaisen Pear (Pyrus communis) Ring spot - Kirk et al., 2008
Rice (Oryza sativa) Leaf spot Pakistan Akhtar et al., 2014
A. grandis Potato (Solanum tuberosum) Early blight Brazil Rodrigues et al., 2010
A. gossypina Cotton (Gossypium hirsutum) Leaf spot and boll rot - Hopkins, 1932
A. helianthi Sunflower (Helianthus annuus) Stem and foliar blight Louisiana Singh & Ferrin, 2012
A. helianth- Sunflower (Helianthus annuus) Leaf spot Korea Cho and Yu, 2000
inficiens Sunflower (Helianthus annuus) Foliar and Stem Blight Croatia Vrandecic et al., 2012
A. heveae Rubber Tree (Hevea brasiliensis) Black Leaf Spot China Cai et al., 2014
A. infectoria Wheat (Triticum aestivum) - - Kirk et al., 2008
A. interrupta Potato (Solanum tuberosum) Early blight Iran Taheri et al., 2009
A. iridicola Blackberry-lily Leaf blight Korea Yu et al., 2000
(Belamcanda chinensis)
A. Water hyacinth Leaf blight - Dagno et al., 2011
jacinthicola (Eichhornia crassipes)
A. japonica Cole crops - - Kirk et al., 2008
Arugula (Diplotaxis tenuifolia) Leaf spot Italy Garibaldi et al., 2011
and garden rocket (Eruca vesicaria)
Chinese cabbage (Brassica rapa) Damping-off China Ren and Zhang, 2012
Arugula (Diplotaxis tenuifolia) Leaf spot California Tidwell et al., 2014
A. Largehead atractylodes rhizome Leaf spot China Tan et al., 2012
217Journal of Oilseed Brassica, 6 (2) July., 2015
longipes (Atractylodes macrocephala)
Tobacco (Nicotiana tabacum) - - Kirk et al., 2008
Carrot (Daucus carota) Leaf Blight Israel Vintal et al., 2002
Potato (Solanum tuberosum) Leaf spot Pakistan Shoaib et al., 2014
China Root (Smilax china) Leaf spot China Long et al., 2009
A. molesta Porpoises (Phocoena phocoena) Skin lesions - Kirk et al., 2008
A. multirostrata Rough Mexican clover Blight - Jackson and Simmons,
(Richardia scabra) 1968
A. mali Apple (Malus communis) Necrotic leaf spot Turkey Ozgonen and Karaca,
2005
A. palandui Onion (Allium cepa) leaf blight - Karthikeyan et al., 2005
A. panax Sun King (Aralia cordata) Leaf spot Japan Zhang et al., 2009
Japanese aralia (Fatsia japonica) Leaf blight Europe Garibaldi et al., 2004
Ginseng (Panax ginseng) Blight Australia, Canada, Woodhall and
China, Italy, Japan, Sansford, 2006
Korea, Netherlands,
New Zealand,
Spain, United Kingdom,
United States and
Venezuela
Octopus tree Leaf spot and blight Hawaii Alfieri et al., 1994
(Schefflera actinophylla)
Ginseng (Panax quinquefolius) Leaf spot and blight Hawaii Alfieri et al., 1994
A. passiflorae Passion-Vine (Passiflora) Brown- spot New Zealand Brien, 1940
A. petroselini Fennel (Foeniculum vulgare) Seedling damping-off Netherlands Pryor & Asma, 2007
Parsley (Petroselinum crispum) Leaf blight - Kirk et al., 2008
Chinese Hickory (Carya cathayensis) Leaf Blight China Liu et al., 2013
Fennel (Foeniculum vulgare) Leaf Blight Spain Bassimba et al., 2012
A. porri Leek (Allium) Purple blotch California Koike & Henderson,
1998
Chicory (Cichorium endivia L.) Leaf Spot Argentina Sarasola, 1970
Velvet Bean (Mucuna pruriens) Leaf Spot China Ye et al., 2013
A. radicina Carrot (Daucus carota) Black Rot Michigan Saude & Hausbeck,
2006
A. raphani Chinese radish (Raphanus sativus) Black patches Canada Su et al., 2005
A. saponariae Soapwort (Saponaria) Leaf spot California Koike et al., 1999
A. selini Parsley (Petroselinum crispum) Crown decay - Kirk et al., 2008
A. sesami Sesame (Sesamum) Leaf spot - Kirk et al., 2008
A. sesamicola Sesame (Sesamum indicum) Blight - Singh et al., 1980
A. smyrnii Alexander (Smyrnium olusatrum) Leaf spot - Kirk et al., 2008
A. solani Potato (Solanum tuberosum) Early blight Idaho Wharton et al., 2012
Potato (Solanum tuberosum) and Early blight - Kirk et al., 2008
tomato (Solanum lycopersicum)
218 Journal of Oilseed Brassica, 6 (2) July., 2015
Potato (Solanum tuberosum) Early Blight Idaho Miles et al., 2013
A. tenuissima Pigeonpea (Cajanus cajan) Blight India Sharma et al., 2012
Siberian Ginseng Leaf spot China Gao et al., 2011
(Eleutherococcus senticosus)
Strawberry (Fragaria) Fruit rot Korea Lee et al., 2001
Broad bean (Vicia faba) Leaf spot Japan Honda et al., 2001
Blueberry disease Leaf spot China Luan et al., 2007
(Vaccinium myrtillus)
Candytuft (Iberis sempervirens) Leaf spot Italy Garibaldi et al., 2005
Leopard Plant Leaf spot Korea Lee et al., 2013
(Farfugium japonicum)
Apple (Malus communis) Postharvest Decay United States Kou et al., 2014
Green Amaranth Leaf Spot - Blodgett et al., 1999
(Amaranthus hybridus)
Potato (Solanum tuberosum) blight China Zheng & Wu, 2013
Blueberry (Vaccinium corymbosum) Leaf spot Western Australia You et al., 2014
A. tomatophila Tomato (Solanum lycopersicum) Early blight Brazil Rodrigues et al., 2010
A. triticimaculans Wheat (Triticum aestivum) Leaf spot Argentina Kirk et al., 2008
Wheat (Triticum aestivum) Leaf spot Argentina Perello et al., 1996
A. yaliinficiens Ya Li pear (Pyrus) Leaf spot U.S Roberts, 2005
A. zinniae Zinnia (Zinnia elegans) Leaf spot Germany Pape, 1942
A. zinniae Marigold (Tagetes patula) Spot and - Chandel and Singh,
flower blight 2010
A. sp. Strawberry (Fragaria) Fruit rot Taiwan Ko et al., 2008
Barberry (Berberis) Stem spot Iran Mairabadi et al., 2005
Highbush Blueberry Leaf spot South Korea Kwon et al., 2014
(Vaccinium corymbosum)
Apple (Malus communis) Leaf blotch Australia Harteveld et al., 2014
Tea plant (Camellia) Leaf spot Italy Garibaldi et al., 2007
Japanese Plum (Prunus) Leaf spot Korea Kim et al., 2005
Loquat (Eribotraya japonica) Fruit Rot Taiwan Ko et al., 2010
Hazelnut (Corylus avellana) Leaf spot - Belisario et al., 2004
and Walnut Fruit (Juglans regi)
219Journal of Oilseed Brassica, 6 (2) July., 2015
Host selective toxins
Disease determinants of Alternaria spp.
Alternaria species being most ubiquitous and
saprophytic fungi produces toxins (Rotem, 1994).
Determination of the exact mode of action of
phytotoxic compounds in pathogenesis or virulence
is critical and it can be determined by studying
virulence and sensitivity of toxins produces by
different isolates on host genotypes (Strange, 2007,
Meena et al., 2012). Recently, Rotondo et al. (2012)
compared the Alternaria spp. collected in Italy with
A. mali (Roberts) and other AM-toxin producing
strains and suggested that the production of the AM-
toxin might be involved in pathogenesis by some of
the Italian isolates of A. alternata.
Host-selective toxins (HSTs) are mycotoxins which
are often essential for both host specificity and
pathogenicity, whereas the non-selective toxins
(NSTs) are mycotoxins which are important only
for virulence. HSTs are produced during germination
of spores on plant surfaces (Mausunaka et al.,
2005). HSTs are generally low-molecular-weight
secondary metabolites but many HSTs like Ptr ToxA
and Ptr ToxB by Pyrenophora tritici-repentis
(Died.) Drechsler, Sn Tox1 and Sn ToxA by
Stagonospora nodorum (E. Mull.) Hedjar and AB
toxin by A. brassicicola (Schw.) Wiltsh, are
proteinaceous in nature (Wolpert et al., 2002, Friesen
et al., 2007, Manning et al., 2009).
Other HSTs are AP- toxin by Alternaria panax
(Whetzel) (Quayyum et al., 2003), destruxin B &
ABR toxin by A. brassicae (Berk.) Sacc. Maculosin
& AS toxin by A. alternata (Fr.) Kressler . Tomato
pathotype of Alternaria alternata produce two
forms of AAL-toxins which are mono-esters of
propane-1,2,3 tricarboxylic acid (TA) and
2,4,5,13,14- pentahydroxyheptadecane (TB) (Wang
et al., 1996). Alternaria alternata pathotypes
Japanese pear, Strawberry, tangerine, rough lemon,
and apple, respectively, produce AK toxin I and II,
AF- toxin I, II and III, ACT- toxin Ib and IIb, ACR
toxin , and AM-toxin. Host- specific toxins
responsible in causing plant diseases are listed in
table 2.
In a study on pathogenic- HST- producing and non-
pathogenic- NST- producing A. alternata
pathotypes, it was revealed that only the pathogenic
pathotypes carried small extra chromosomes
(Akamatsu et al., 1999, Thomma, 2003). All the
toxins produced by A. alternata pathotypes are
similar in structure. Genes associated with the
synthesis of AK, AF and AM toxins are clustered
together on small chromosomes (Tanaka & Tsuge,
2000, Johanson et al., 2000; 2001, Hatta et al.,
2002). Many mutants have been included in
studies determining involvement of toxin in disease
development. Johanson et al. (2000) cloned and
sequenced the cyclic peptide synthetase gene
responsible in the synthesis of AM-toxin; this gene
has no introns and is 13.1 Kb in length. Mutants
obtained by transformation of a wild type toxigenic
isolate with disruption vectors were toxin-minus
which were unable to cause disease symptoms on
susceptible apple cultivars. Recovery of genomic
DNA flanking the integration site revealed two genes
ak1 & ak2. ak1 encodes a carboxyl activating
enzyme, while ak2 encodes a protein of unknown
function. Targeted gene disruption showed that both
ak1 and ak2 genes were necessary for pathogenicity
and toxin production. Homologues of both genes
were detected in both tangerine and pear pathotypes,
but not in other pathotypes or non-pathogenic isolates.
Several other mycotoxins and phytotoxic
metabolites produced by Alternaria species include:,
Alternaric acid, alternariol, solanapyrone and
zinnolide by A. solani (Ellis & G. Martin) (Anderson
et al., 2008), Alternariol monomethyl ether by A.
dauci (J.G. Kuhn) (Ostry, 2008), erythroglaucin and
anthraquinones by A. porri (Ellis). Ciferri (Ostry,
2008), ATC-toxin by A. tenuissima (Kunze)
Wiltshire (Ostry, 2008), and zinnolide and znnimidine
by both A. solani (Sorauer) and A. cichorii
(Natrass) (Ostry, 2008). Zinnolide and Znnimidine
are structurally similar to Zinnole which is the only
common metabolite produced by A. porri, A. dauci
and A. solani (Horiuchi et al., 2003). Alternaric acid,
produced by A. solani, although not phytotoxic when
sprayed alone on tomato leaves, but it is the major
metabolite responsible for the development of
necrotic and chlorotic symptoms. Alterporriols,
altersolanols, macrosporin and tentoxin are produced
220 Journal of Oilseed Brassica, 6 (2) July., 2015
Table 2. A list of Host-specific toxins and their diseases
Disease Pathogen species Toxin Target site Chemical structure References
Alternaria stem Alternaria alternata f.sp. lycopersci AAL-Toxin Sphingolipid & Ester of propanetricarboxylic acid Bottini and Gilchrist,
cancker of (tomato pathotype) ethanolamine and aminodimethylheptad 1981
tomato metabolism ecapentol
Brown spot of Alternaria alternata f.sp. citri ACT toxin Plasma membrane Ester of amino acid Kohmoto et al., 1993
tangerine tangerine epoxydecatrienoic acid
Black leaf spot Alternaria alternata f.sp. fragariae AF toxin Plasma membrane Ester of amino acid Nakatsuka et al., 1986
of strawberry (strawberry pathotype) epoxydecatrienoic acid
Black leaf spot Alternaria alternata f.sp. kikuchiana AK toxin Plasma membrane Ester of amino acid Nakashima et al., 1985
of Japanese pear (Japanese pear pathotype) epoxydecatrienoic acid
Brown spot of Alternaria alternata f.sp. citri jambhiri ACR toxin Mitochondria Polyhydroxyalkenyl Gardner et al., 1985
rough lemon (rough lemon pathotype) I dehydropyrone
Alternaria blotch Alternaria alternata f.sp. mali AM toxin Chloroplast and Cyclic depsipeptide Okuno et al., 1974
of apple (apple pathotype) plasma membrane
-Alternaria alternata (spotted Maculosin - - Stierle et al., 1988
knapweed pathogen)
-Alternaria alternata AS-toxin - - Liakopoulou-
(sunflower pathogen) kyriakides et al., 1997
Black spot of Alternaria brassicae Destruxin B - cyclidepsipeptide Bains & Tiwari, 1987
rapeseed
Black leaf spot Alternaria brassicicola AB-toxin - Protein Chaube & Pundhir,
of Brassica spp 2005
Brown spot of Alternaria alternata Tobacco AT -toxin - - Chaube & Pundhir,
Tobacco pathotype (A. longipes)2005
-Alternaria brassicae ABR-toxin - - Parada et al., 2008
Alternaria panax AP-toxin - - Quayyum et al., 2003
221Journal of Oilseed Brassica, 6 (2) July., 2015
in cultures of A. porri and A. solani (Suemitsu et al.,
1992). Alternaria alternata produces a number of
mycotoxins, including alternariol, alternariol
monomethyl ether, altenuene, altertoxins I, II, III,
and tenuazonic acid (Ostry, 2008, Zhou & Qiang,
2008). Nine novel compounds closely related to
ACTG-toxin, termed as tricycloalter-narenes, were
isolated from a strain of A. alternata, from B.
sinensis (L.) which was earlier used for the
production of the non-specific phytotoxin tentoxin
(Nussbaum et al., 1999). Liebermann et al. (2000)
also reported isolation of 11 new bicycloalternarenes
as well as ACTG-toxins A and B. Alternaria
brassicae (Berk.) Sacc. produces cyclic
depsipeptide phytotoxin including Homodestuxin B,
Destruxin B2 & desmethyldes-truxin B (Ayer &
Pena-Rodriguez, 1987, Buchwaldt & Green, 1992,
Montemurro & Visconti, 1992, Agarwal et al., 1994,
Parada et al., 2008). Alternaria brassicicola
produces despeptides and fucicoccin-like toxic
compounds and also proteinaceous Brassicillin A
(Pedras et al., 2009, Cooke et al., 1997, MacKinnon
et al., 1999).
Mode of action of HST’s
Understanding the mechanism of action of HSTs
provide a better picture of host pathogen
interactions and resistance mechanisms. Of the two
approaches used to study the mode of action of
pathogen, one is the study of host selectivity at the
molecular level, and the other at the cellular level.
Hypersensitive response (HR) is one of the most
effective defense mechanisms developed by plants
against their pathogens where several pathogenesis-
related proteins (PR) participate and necrosis of the
tissue at the site of infection and formation of
phytoalexins occur (Agrios, 2005).
At Physiological level
The effect of phytotoxins on plants at the
physiological level is characterized by the malfunc-
tioning of many physiological processes including
respiration, transpiration, photosynthesis, translocation,
growth and development. It is also characterized by
the appearance of specific symptoms including
wilting, growth suppression, chlorosis, necrosis, and
spotting of aerial portions.
Physiological processes
Alternaria HSTs are classified into three groups in
terms of primary site of action. AM toxin targets
the chloroplast and plasma membrane, ACR (L) toxin
targets mitochondria and ACT, ACTG, AK, AF
toxins target the plasma membrane (Fig. 1).
A. solani infection in potato decreases
photosynthesis and increases respiration, in both
necrotic and adjacent symptomless tissues (Livescu
et al., 1986). In general, respiration increases once
parasitic relationships is established. Alternaria
pathogens infect green aerial tissues and reduce
photosynthetic activity, produce cytokinins which
lead to the formation of Green Island below the
germinating conidia on senescing tissues, and cause
deformation in chloroplast and mitochondria
(Chaturvedi, 1972, Agarwal et al., 1994, Zheng et
al., 2006). In tobacco, treatment by A. alternata
produced metabolites decrease chlorophyll content,
soluble protein, photosynthetic O2 production,
catalase activity, and increase in H2O2 content in
the senescence leaves (Jia et al., 2010). Plasma
membrane is a common active site for action of
toxins in animal and plant cells. Alternaria macrospora
(Zimm.) alters plasma membrane permeability in
leaves, and increases leakage of electrolytes, mainly
potassium ions (Park & Ikeda, 2008). In Brassica
juncea, A. brassicae HST destruxin B inhibits
almost all-macromolecular biosynthesis, promotes ion
leaching, and causes aberrations in mitochondria and
chloroplast. In tomato, Alternaria solani produced
alternaric acid induces physiological and morpho-
logical modifications of the plasma membrane near
plasmodesmata; modification includes localization of
free ions in the vicinity of plasma membrane
invaginations (Langsdorf et al., 1991).
Specific symptoms
Toxins produced by A. brassicae cause brown
necrotic spots on leaves and brown streaks on stem
leading to yield losses (Aneja & Agnihotri, 2013).
Alternaria raphani (Groves & Skolko) produces
black stripes or dark brown, sharp-edged lesions on
the hypocotyls of the seedling (Valkonen &
Koponen, 1990) whereas, A. brassicicola produces
black sooty velvety spots. Alternaria infection
reduces size of leaves and number of flowers in
222 Journal of Oilseed Brassica, 6 (2) July., 2015
tomato (Coffey et al., 1975), and stimulates shedding
of infected leaves (Spross-blickle et al., 1989).
At Biochemical level
Infection of Plants by pathogenic fungi may trigger
several biochemical defense responses including
enzyme synthesis, cell wall deposition of lignin and
suberin, and accumulation of speciûc metabolites
(Daayf & Platt, 2000, Abdel-Farid et al., 2009). The
mechanisms of host selective pathogenesis are not
well understood at the biochemical level, even in
cases where the toxin site of action is known.
Enzyme synthesis
The first physical barrier between plants and
pathogen invasion is the cuticle (Schweizer et al.,
1996, Fan & Koller, 1998, Farah et al., 2005) and
cell wall, which inhibit both initiation and spread of
infection. One characteristic feature of many
phytopathogenic organisms is their ability to produce
an array of extracellular and highly stable enzymes
capable of degrading the complex polysaccharides
of the plant cell wall and membrane constituents.
Inoculation of A. brassicae on the leaves of
B. juncea blight resistant cultivar RC-781 decreases
the activities of cell wall degrading polygalcturonase
and cellulose enzymes, but increases their activities
in a sucepticible cultivar Varuna up to 3 days of
infection (Garg et al., 1999). Infection of
A. brassicicola shows a differential and sequential
induction of two classes of cutinolytic esterases. One
class is expressed only in short duration contact
(24hr) with intact cutin, but not induced by cutin
monomer. The second class however, is induced by
cutin monomers only in prolonged exposure with
intact cutin. This differential behavior indicates a
sequential recognition of cutin as a barrier to be
penetrated and utilized as a carbon source in
Fig.1. Schematic representation of changes at physiological level by Alternaria spp.
(Source : Park et al., 1976; Akimitsu 1989; Otani et al., 1995; Thomma 2003; Park and Ikeda 2008 )
223Journal of Oilseed Brassica, 6 (2) July., 2015
saprophytic stages. (Yao & Koller, 1995, Fan &
Koller, 1998, Baker et al., 2005). The small (7-10
KD), lipid transfer proteins (LTPs) are expected to
be involved in wax transport because of their
increased expression during drought condition
(Beisson et al., 2003, Cameron et al., 2006, Jubert
et al., 2011). During A. brassicicola infection the
ltpg1 (GPI-anchored LTP) knockout mutant showed
increased susceptibility (Lee et al., 2009), but the
genetically unidentified cutinase- deficient mutants
were non pathogenic (Tanabe et al., 1988). Suzuki
et al. (2003) observed that during citrus-pathogen
A. alternata infection, cutinase release from pegs
functions as an aggressiveness factor for penetration
into pear tissues ( Perez et al., 1991), and triggers a
hypersensitive response (HR) in lemon seedlings
characterized by phenylalanine ammonia–lyase
induction (Roco et al., 1993), scoparone synthesis
(Perez et al., 1994a), tissue maceration (Perez et
al., 1994b), participation in a signaling pathway
including calmodulin, G protein and protein kinases
(Ortega & Preze, 2001), and phosphoinositide
metabolism (Ortega et al., 2002). It was observed
that the expression of hsr203j gene, a known marker
for hypersensitive response is more in A. brassicae
tolerant cultivar than in susceptible cultivar of
B. juncea (Mishra et al., 2011). Chitin is a component
of fungal cell walls, which is absent in plants, yet
plants produce chitin–degrading enzymes; chitinase
produced in plants can directly affect the viability of
fungal pathogens (Boller, 1995, Stacey & Shibuya,
1997, Shibuya & Minami, 2001). This is proved by
overexpression of chitinase in transgenic plants
which are generally more resistant to fungal
pathogens. Further, it was observed that more
chitinase is produced and accumulate at the site of
fungal infection (Majeau et al., 1990, Roby et al.,
1990, Wubben et al., 1992). Chikkara et al. (2012)
reported that co-expression of chitinase and ribosomal
- inactive protein in B. juncea provides more
protection against A. brassicae. AAL-toxin,
structurally related to sphinganine, a member of
sphinganine-analogue mycotoxin (SAMS), is an
inhibitor of sphinganine-N-acyltransferase (Gilchrist
et al., 1994, Abbas et al., 1994) enzyme important
in sphingolipid biosynthesis leading to accumulation
of free sphingoid bases (Brandwagt et al., 2000,
Spassieva et al., 2002, Gechev & Hille, 2005). These
long chain sphingoid bases (LCBs) are determinant
in the occurrence of programmed cell death (PCD)
in susceptible plants (Shi et al., 2007, de Zélicourt
et al., 2009). SAMS inhibit ceramide biosynthesis.
Biochemical and molecular data demonstrated that
programmed cell death (PCD) triggered by AAL-
toxin is also associated with H2O2 (Gechev et al.,
2004) as atr mutant of Arabidopsis show enhanced
tolerance to H2O2 and reactive oxygen species
(ROS) - induced cell death (Gechev & Hille, 2005,
Gechev et al., 2008). Brassinin hydrolases, a
detoxifying enzyme (BHAb) of a crucifer phytoalexin
brassinin, also plays an important role in
development of disease caused by A. brassicicola
in Brassica (Pedras et al., 2009).
Accumulation of specific metabolites
In Japanese pear, although infection by A. alternata,
induces general resistance by increasing release of
polysaccharides (Hayami et al., 1982), its AK
toxins increase susceptibility in cultivar Nijisseiki by
suppressing production and release of polysaccharides
(Otani et al., 1991, Kodama et al., 1998, Suzuki et
al., 2003). In Chinese cabbage, A. brassicae
infection signiûcantly increases glucosinolates
(aliphatic and indole) and anthocyanins, but
decreases sucrose levels (Rosta´s et al., 2002,
Abdel-Farid et al., 2009). Imazaki et al. (2010)
reported that A. alternata pathotypes contain
abundant peroxisomes which are very important in
both tissue colonization and pathogenesis. Other
functions of peroxisomes include fatty acid
metabolism, acetyl-CoA generation, secondary
metabolism, cell wall biogenesis, and peroxisome
homeostasis.
At Molecular level
The interaction between plants and pathogens at
molecular level are specific, complex and dynamic.
Many responses are evoked in plants upon
encountering pathogens, but relatively very few have
been studied in detail. Key events in plant-pathogen
interaction include perception of pathogen on the
plant or cell surface by receptors/sensors, and
transduction of these perceptions through various
transcription factors and target genes which are
involved in coordination of the appropriate responses
(Hammond & Jones, 1996). Different types of both
224 Journal of Oilseed Brassica, 6 (2) July., 2015
plant and pathogen genes have been shown to be
involved in plant and necrotrophic fungal interaction.
These responses range from genes that encode
proteins like receptor/receptor kinase, cell wall
degrading enzymes, toxins, and transporter proteins,
to those involved in signal transduction cascades
such as mitogen activated protein kinases (MAPKs),
and various transcription factors like WRKY, NAC
(Lawrence et al., 2008, Wang et al., 2009, Amselem
et al., 2011). Ghose et al. (2008) also studied the
differential profiling of selected defense-related
genes induced on challenge by A. brassicicola in
resistant white mustard, and their comparative
expression pattern in susceptible Indian mustard.
These genes have similarity with receptor-like-
protein-kinase genes, genes involved with calcium-
mediated signaling, salicylic acid-dependent genes,
and other functional genes in Arabidopsis. Various
studies determining the role of receptor/receptor-
like- protein in perception of fungal pathogens have
been concluded. After the attack, the fungal cell
wall is hydrolyzed by an enzyme chitinase, and
fragment of cell wall chitin is perceived by a receptor
known as chitin elicitor receptor kinase (CERK1)
or Lys M receptor-like protein kinase (Lys M
RLK1). A mutation in lys m gene blocks the induction
of almost all chito-oligosaccharide-responsive genes
and leads to increased susceptibility to fungal
pathogens indicating that LysM RLK1 is essential
for chitin signaling in plants (Wan et al., 2008).
Another receptor gene, Phytosulfokine Receptor
(PSK-receptor) psk2 and pskr1, also got induced in
Arabidosis leaves after A. brassicicola infection,
which shows its role in pathogenesis (Loivamaki et
al., 2010).
Phytopathogenesis of A. brassicae on B.
juncea
Molecular mechanism of Alternaria blight in
Brassica shows involvement of chlorotic & necrotic
toxins as well as of phytohormone. Alternaria
brassicae produces a chlorotic toxin destruxin B
that plays an important role in signal transduction
leading to programmed cell death, and suppressing
the defense system (Taj et al., 2004). Differential
expression of cell cycle proteins in toxin- treated
leaves and calli, and overexpression of p53 suggest
that the toxin-mediated perturbations in cell cycle
eventually cause p53- induced - programmed cell
death (PCD) (Khandelwal et al., 2002).
Interestingly, A. brassicae pathotoxin-induced-cell-
death pathway was antagonized by a phytohormone
zeatin, in cell culture of B. juncea (Pandey et al.,
2001). The antagonistic effect of these two
structurally different entities strongly suggests the
role of interactive- signaling -pathways in pathogenesis
of Alternaria blight in Brassica species.
Introgression of Osmotin, a known pathogenesis
related PR-5 protein causes perturbation in resistance
to biotic and abiotic stresses (Taj et al., 2004). The
effect of toxin and zeatin treatments on the
B. juncea leaf proteome was investigated by using
two-dimensional electrophoresis and liquid
chromatography mass spectrometry (LCMS)
techniques; results showed that 20 proteins were
uniquely expressed in toxin treated leaf, while 27
proteins were expressed in together with toxin and
zeatin. LCMS technique has also been used to
identify a total of 15 proteins with differential
expression in toxin treated leaves. The proteins
identified in response to the toxin are glycosyl
hydrolases, subtilisin like proteases, P-nitrophenyl
phosphatase, malate dehydrogenase, heat shock,
ribulose 1,5 bis phosphate carboxylase, Cucumisin-
like serine proteases, Globulin like protein, and
adenosine triphosphate (ATP) synthase (Singh et al.
unpublished data). Shrama et al. (2007) also
studied the proteome –level changes in A. brassicae
– B. napus and suggested role of reactive oxygen
species (ROS)- mediated- auxin- signaling in the
pathosystem.
Mitogen-activated-protein-kinases (MAPK)
cascades are also standard players in the signal
transaction literature for diverse organisms (Madhani
& Fink, 1998, Cobb, 1999). Activation of MAPK
confers resistance to both bacterial and fungal
pathogens (Sheen et al., 2002). Deciphering the
MAP Kinase machinery components in B. juncea,
reverse transcriptase polymerase chain reaction
(RT-PCR) amplification of all 20 known MAPK has
been done. Amongst the MAP Kinases 8, 12 and 18
showed no expression, expression of MAP Kinase
3, 10 and 14 were validated with the Northern Blot
(Singh et al. unpublished data), MAPK 3 important
gene directly correlated with the transcription
225Journal of Oilseed Brassica, 6 (2) July., 2015
factors, and expresses in compatible interaction of
A. brassicae and B. juncea (Taj et al., 2011).
Expression of MAPKK4, MAPKK5, MAPKK9,
MAPKKK1, Wrky 22 and Wrky 29 has also been
validated by Real time PCR (Giri et al., unpublished
data). Expression analysis of MAP 2K 9 and MAP
K 6 is also governed during pathogenesis of
Alternaria blight in A. thaliana. where simultaneous
increased levels up to middle stage of disease
progression were observed (Kannan et al., 2011).
Deciphering the resistance mechanism in Basella
alba (L.), against A. brassicicola shows the down-
stream signaling of MAPK-6 which was found to
be activated after ethylene treatment (Taj et al.,
2010). This might be a significant step as up-regula-
tion of ndr1/hin-1- like gene nhl25, and PR gene
reported during Basella alba infection (Varet et al.,
2002); these genes were downstream targets of
MAPK6 in Arabidopsis which are controlled by
Salicylic acid (SA) (Desikan et al., 1999, Ghose et
al., 2008). Activation of more than one member of
MAPK by Alternaria suggests that MAPK
cascades act as points of convergence and
divergence in signaling, and might play a pivotal role
in deciding whether disease should progress, or
defense pathways defeat the pathogen. Transgenic
potato plants carrying StMEK1 (MAPKK) also
show resistance against A. solani by provoking
oxidative burst-mediated plant defense (Yamamizo
et al., 2006).
Phytohormones in Alternaria pathogenesis
The involvement of phytohormone dependent
pathway is well documented in plant pathogen
interaction. Role of Jasmonic acid (JA)- dependent-
signaling- pathway of necrotrophic pathogen, and
Salicylic acid (SA) –dependent- signaling- pathway
of biotrophic pathogen is also well documented.
Mutants of JA, and/or Ethylene (ET)- signaling
pathways, and JA-insensitive coi-1 of A. thaliana
respectively, show increased susceptibility, and
resistance against A. brassicicola (Thomma et al.,
1999, Kachroo et al., 2001, Nandi et al., 2005, Mang
et al., 2009). Systemic expression of the JA-
inducible pdf1.2 gene is also reduced after infection
with A. brassicicola. This reflects the necessity of
JA-mediated responses for expression of this trait
(Glazebrook, 1999). In contrast, the SA-insensitive
mutant npr-1, and SA-depleted nahG line has no
effect on the resistance phenotype (Thomma et al.,
1998) indicating no direct involvement of SA as a
signaling molecule. In another study, induction of SA
signaling marker, PR1, and enhanced biosynthesis
of the antifungal compound camalexin upon
infection by A. brassicicola in Arabidopsis raises
the possibility of cross-talk between these different
signaling networks (Doares et al., 1995, Kunkel &
Brooks, 2002, Kachroo et al., 2003a, 2003b). Over-
expression of ngnpr3 gene in tobacco plant also
shows the resistance against A. brassicicola (Zhang
et al., 2010). Jasmonic acid also helps in the
modulation of MAP Kinase 4 and MAP Kinase 6
during phytopathogenesis of Alternaria blight in
A. thaliana.
Furthermore, biosynthesis of antifungal compounds
camalexin which plays a role against Alternaria
pathogen has been found to be positively controlled
by SA and ET. JA regulated lox gene is also known
to play role during A. brassicae pathogenesis (Taj et
al., 2011). During incompatible interaction of
Arabidopsis transgenic plant harboring CaLOX1-
OX, lox1 mutant and A. brassicicola, it was
discovered lox1 mutant plants are more susceptible
than wild type, CaLOX1-OX transgenic, and
CaLOX1 plants (Hwang & Hwang, 2010).
Transcription of the plant defense genes pdf1.2 and
Thi2.1 is enhanced in response to Botrytis cinerea
(De Bary) Whetzel and A. brassicicola infection,
and is dependent on ET, JA, and Oleic Acid (OA)
signals (Epple et al., 1995, Penninckx et al., 1996,
Kachroo et al., 2003a, 2003b). Resurrection1 (rst1)
mutant plants show more resistance to the
necrotrophic fungi Botrytis cinerea and
A. brassicicola by suppressing pathogen growth,
sporulation, and disease symptoms, which might be
due to altered cuticular waxes (Chen et al., 2005),
because the amount of cutin monomers,
phytoalexin accumulation, and basal expression of
the pdf1.2 gene were significantly enhanced in
infected leaves (Mang et al., 2009). Unlike rst 1
mutation, other mutations including mpk4, bik1 and
wrky33, cause susceptibility to the necrotrophic
pathogens A. brassicicola and Botrytis cinerea
(Petersen et al., 2000, Wiermer et al., 2005,
226 Journal of Oilseed Brassica, 6 (2) July., 2015
Veronese et al., 2006, Zheng et al., 2006, Mang et
al., 2009). Constitutive expression of VvWRKY2
in tobacco reduces susceptibility of A. tenuis to the
seeds of transgenic tobacco (Mzid et al., 2007).
DEAD-box RNA helicase also plays role during
Arabidopsis- A. brassicicola interaction.
Transgenic Arabidopsis plant that over-expresses
the osbirh1 gene (DEAD-box RNA helicase
protein) also shows enhanced expression of PR-1,
PR-2, PR-5, PDF1.2, and disease resistance against
A. brassicicola (Li et al., 2008).
At the cellular level, events during the infection by
A. solani include general defense responses found
also in other plant–pathogen interactions
involving quantitative resistance. These responses
are basically similar to hypersensitive responses in
monogenic resistance, but they are expressed more
slowly and at a lower level (Agrios, 2005, Chaerani
& Voorrips, 2006).
Differential expression of genes in pathogen
During the course of infection, various genes of
pathogen are also expressed and play role in fungal
pathogenesis. Gene aafus3 which encodes for
FUS3MAPK in A. alternata is required for conidial
development and penetration of the fungus in plant
(Lin et al., 2010). Another study shows that
deletion of abpro1 (transcription factor) and abnik1
(two component histidine kinase) gene of
A. brassicicola results in 70 % and complete loss
of virulence, respectively (Cho et al., 2009).
Cyanide hydralase, arsenic ATPase, formate
dehydrogenase, are some other genes of
A. brassicicola which are being expressed, and
have a role in fungal pathogenesis (Cramer &
Lawrance, 2004). Recently, one group shows that
unfolded protein response (UPR) pathway also
regulates the fungal pathogenesis, and abhac a gene
encodes the major UPR transcriptional regulator;
Loss of UPR in mutants of A. brassicicola resulted
in complete loss of virulence (Joubrt et al., 2011).
Future Aspects
The physiological, biochemical and molecular basis
for resistance toward Alternaria pathogens is still
mostly unknown despite recent advancements.
There are still many uncovered distinct signaling
pathways, enzymes and key regulatory factors
involved in this process. Further studies on plant-
Alternaria interaction require uncovering the
different mechanisms employed by the pathogen to
develop disease, and overpower the plant defense
system. No doubt, these studies will promote our
understanding of pathogenesis, and may provide
clues to manipulate plant defense signaling pathways
as resistance against this fungus, is controlled by
multiple plant defense pathways, including both
constitutive and inducible factors. Our objective in
this review was to provide an overview of
physiological, biochemical and molecular basis of
phytopathogenesis of Alternaria species. Future
work should focus on understanding the complete
picture of Alternaria spp. complex affecting
individual vegetable/ Brassica crops with very host-
specific Alternaria species to elucidate the
physiology of the early steps involved in signal
recognition. There is also a need to study the
relationship between pathogenic and molecular
(sequence) variability among Alternaria isolates
apart from relation with morphological and cultural
data. Based on the sequence data of type culture,
host differentials also need to be standardized.
Acknowledgments
This review is respectfully dedicated to Dr. G. K.
Garg, who provided the opportunity to review the
pathogenesis mechanism of A. brassicae, and to
appreciate his eminent way of thinking about
A. brassicae - Brassica interaction and his sincere
and dedicated attitude towards research. The
authors are also greatful to Dr. P.R. Verma, Bipasha
Sarkar and Bijal Chokshi for editing the manuscript.
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... Scott (2001) reported that A. alternata is a frequently occurring species in field and storage and produces a number of mycotoxins, including alternariols (AOH, AME, and ALT) and TeA. The exposure of pathogen or its toxic metabolites disturb the normal physiological processes like photosynthesis, respiration, translocation, transpiration, growth and development and characterized by major biochemical changes that include the synthesis of antioxidative defense enzymes and accumulation of specific metabolites (Taj et al., 2015). Pathogen or toxins induced cell damages could be manifested in the form of specific symptoms including wilting, growth suppression, chlorosis, necrosis, and spotting of aerial portions. ...
Article
Full-text available
In the present study, we have evaluated the comparative biochemical defense response generated against Alternaria alternata and its purified toxins viz. alternariol (AOH), alternariol monomethyl ether (AME), and tenuazonic acid (TeA). The necrotic lesions developed due to treatment with toxins were almost similar as those produced by the pathogen, indicating the crucial role of these toxins in plant pathogenesis. An oxidative burst reaction characterized by the rapid and transient production of a large amount of reactive oxygen species (ROS) occurs following the pathogen infection/toxin exposure. The maximum concentration of hydrogen peroxide (H2O2) produced was reported in the pathogen infected samples (22.2-fold) at 24 h post inoculation followed by TeA (18.2-fold), AOH (15.9-fold), and AME (14.1-fold) in treated tissues. 3,30- Diaminobenzidine staining predicted the possible sites of H2O2 accumulation while the extent of cell death was measured by Evans blue dye. The extent of lipid peroxidation and malondialdehyde (MDA) content was higher (15.8-fold) at 48 h in the sample of inoculated leaves of the pathogen when compared to control. The cellular damages were observed as increased MDA content and reduced chlorophyll. The activities of antioxidative defense enzymes increased in both the pathogen infected as well as toxin treated samples. Superoxide dismutase (SOD) activity was 5.9-fold higher at 24 h post inoculation in leaves followed by TeA (5.0-fold), AOH (4.1-fold) and AME (2.3-fold) treated leaves than control. Catalase (CAT) activity was found to be increased upto 48 h post inoculation and maximum in the pathogen challenged samples followed by other toxins. The native PAGE results showed the variations in the intensities of isozyme (SOD and CAT) bands in the pathogen infected and toxin treated samples. Ascorbate peroxidase (APx) and glutathione reductase (GR) activities followed the similar trend to scavenge the excess H2O2. The reduction in CAT activities after 48 h post inoculation demonstrate that the biochemical defense programming shown by the host against the pathogen is not well efficient resulting in the compatible host􀀀pathogen interaction. The elicitor (toxins) induced biochemical changes depends on the potential toxic effects(extentofROSaccumulation,amountofH2O2produced).Thus,afinetuningoccursforthedefenserelatedantioxidativeenzymesagainstdetoxificationofkeyROSmoleculesandeffectivelyregulatedintomatoplantagainstthepathogeninfected/toxintreatedoxidativestress.ThestudywelldemonstratestheacutepathologicaleffectsofA.alternataintomatooveritsphytotoxicmetabolites.
... In Alternaria-Brassica host-pathosystem following categories of variability exists, Although, the genus Alternaria is known as an imperfect fungus, it shows genetic variability within a species. This variability might be due to the existence of mutation, somatic hybridization, hetero-karyoses, uniform host selection, extensive dispersal or of a cryptic sexual stage (Gohar Taj et al., 2015). Out of four species of Alternaria known to occur on crucifers, Alternaria brassicae (Berk.) ...
Technical Report
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Training addressed the recent advances in oilseed Brassica plant pathology particularly on various aspects of plant disease management through lectures, practical and field visits. Scientific areas covered including diagnostics, IDM, pathogen diversity, epidemiology, resistance breeding, cultural practices, conventional and molecular approaches etc. We are highly grateful to Prof. Arvind Kumar, Hon’ble Vice Chancellor, Rani Lakshmi Bai Central Agricultural University, Jhansi for his constant support, guidance and encouragement in making the training a great success. We gratefully acknowledge the help and guidance received from Dr. N.S. Rathore, DDG (Edn) & Dr. M. B. Chetti, ADG (HRD), ICAR. We would be failing in our duty if we do not put on record the help and guidance received from Dr. Dhiraj Singh, Director, DRMR in conducting the proceedings of the training through practical and field visits.
Article
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Alternaria causes pathogenic disease on various economically important crops having saprophytic to endophytic lifecycle. Pathogenic fungi of Alternaria species produce many primary and secondary metabolites (SMs). Alternaria species produce more than 70 mycotoxins. Several species of Alternaria produce various phytotoxins that are host-specific (HSTs) and non-host-specific (nHSTs). These toxins have various negative impacts on cell organelles including chloroplast, mitochondria, plasma membrane, nucleus, Golgi bodies, etc. Non-host-specific toxins such as tentoxin (TEN), Alternaric acid, alternariol (AOH), alternariol 9-monomethyl ether (AME), brefeldin A (dehydro-), Alternuene (ALT), Altertoxin-I, Altertoxin-II, Altertoxin-III, zinniol, tenuazonic acid (TeA), curvularin and alterotoxin (ATX) I, II, III are known toxins produced by Alternaria species. In other hand, Alternaria species produce numerous HSTs such as AK-, AF-, ACT-, AM-, AAL- and ACR-toxin, maculosin, destruxin A, B, etc. are host-specific and classified into different family groups. These mycotoxins are low molecular weight secondary metabolites with various chemical structures. All the HSTs have different mode of actions, biochemical reactions, and signaling mechanisms to causes diseases in the host plants. These HSTs have devastating effects on host plant tissues by affecting biochemical and genetic modifications. Host-specific mycotoxins such as AK-toxin, AF-toxin, and AC-toxin have the devastating effect on plants which causes DNA breakage, cytotoxic, apoptotic cell death, interrupting plant physiology by mitochondrial oxidative phosphorylation and affect membrane permeability. This article will elucidate an understanding of the disease mechanism caused by several Alternaria HSTs on host plants and also the pathways of the toxins and how they caused disease in plants.
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Studies were undertaken to determine Alternaria spp. associated with leaf spot symptoms on canola (Brassica napus) in two cropping seasons (2015, 2016) across southern Australia. Major allergen Alt a1 and plasma membrane ATPase genes were used to identify Alternaria spp. In 2015, 112 isolates of 7 Alternaria spp. were obtained, with A. metachromatica predominating. In 2016, 251 isolates of 12 Alternaria spp. were obtained, with A. infectoria predominating. Alternaria spp. isolates were used in morphological and phylogenetic identification; and in studies to determine their pathogenicity on both B. napus (cv. Thunder TT) and B. juncea (cv. Dune) that confirmed 10 species (A. alternata, A. arborescens, A. brassicae, A. ethzedia, A. hordeicola, A. infectoria, A. japonica, A. malvae, A. metachromatica and A. tenuissima) as pathogenic on both Brassica species. A. ethzedia, A. hordeicola and A. malvae constituted first records for Australia on any host, as did A. arborescens for New South Wales (NSW) and South Australia (SA). Other first records included A. infectoria on B. napus in NSW; A. japonica on B. napus in NSW and Western Australia (WA); A. metachromatica on any host in NSW, Victoria (VIC), WA and for SA; and, A. tenuissima on B. napus in NSW, SA and WA. It is evident that Alternaria leaf spot on canola across southern Australia is not solely caused by A. brassicae, but that a range of other Alternaria spp. are also involved to varying degrees depending upon the year and the geographic locality. This article is protected by copyright. All rights reserved.
Article
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Alternaria is an important fungus to study due to their different life style from saprophytes to endophytes and a very successful fungal pathogen that causes diseases to a number of economically important crops. Alternaria species have been well-characterized for the production of different host-specific toxins (HSTs) and non-host specific toxins (nHSTs) which depend upon their physiological and morphological stages. The pathogenicity of Alternaria species depends on host susceptibility or resistance as well as quantitative production of HSTs and nHSTs. These toxins are chemically low molecular weight secondary metabolites (SMs). The effects of toxins are mainly on different parts of cells like mitochondria, chloroplast, plasma membrane, Golgi complex, nucleus, etc. Alternaria species produce several nHSTs such as brefeldin A, tenuazonic acid, tentoxin, and zinniol. HSTs that act in very low concentrations affect only certain plant varieties or genotype and play a role in determining the host range of specificity of plant pathogens. The commonly known HSTs are AAL-, AK-, AM-, AF-, ACR-, and ACT-toxins which are named by their host specificity and these toxins are classified into different family groups. The HSTs are differentiated on the basis of bio-statistical and other molecular analyses. All these toxins have different mode of action, biochemical reactions and signaling mechanisms to cause diseases. Different species of Alternaria produced toxins which reveal its biochemical and genetic effects on itself as well as on its host cells tissues. The genes responsible for the production of HSTs are found on the conditionally dispensable chromosomes (CDCs) which have been well characterized. Different bio-statistical methods like basic local alignment search tool (BLAST) data analysis used for the annotation of gene prediction, pathogenicity-related genes may provide surprising knowledge in present and future.
Article
Aswagandha (Withania somnifera ) is a very important medicinal crop used extensively in Indian Systems of medicine. The crop is now being cultivated commercially under contract farming. The plant is affected severely by leaf blight disease causing leaf drop and resulting in drastic reduction in root yield. Studies were conducted to isolate, characterize and identify the causal organism. Results suggested that the causal organism was Alternaria chlamydospora.
Chapter
Host recognition and its specificity in host-parasite interactions are the most attractive subjects in the field of physiological plant pathology. Recently, several models have been proposed as to the mechanisms responsible for determining disease specificity. One of these models comes from studies of host-specific or host-selective toxins (HSTs) produced by fungal pathogens. A mechanism that determines specificity in the diseases involving HST is comprised of three basic processes (Nishimura et al., 1983; Kohmoto et al., 1987, 1989): 1) Spores of a fungal parasite release HST, a host recognition factor, on germination, 2) the released signal factor selectively binds to receptor sites in the host cells, and 3) the accessible state or susceptibility of host cells to possible hyphal invasion is disposed by the signal transduction.
Article
To determine the action site of the toxin alternaric acid, the ultrastructure of cells of susceptible tomato leaves was observed. Toxin-treated tomato leaves were subjected to conventional electron microscopy and a precipitation method for some types of ions in tissue combined with analytical electron microscopy. The earliest effect of the toxin (10μg/ml) appeared on the plasmodesmatal area where electron-dense precipitates were found at cell walls after 15min exposure time. Afterwards modification of the plasma membrane occurred near the plasmodesmata consisting of slight invaginations which did not expand remarkedly later on. Precipitation of electron-dense substances at cell walls was found at 90% and invagination of the plasma membrane at 60% of the observed plasmodesmatal sites. Magnesium-ions of tissue origin could be determined in these precipitates that indicated leaking of electrolytes. Thus, alternaric acid appears to alter the morphological and physiological characteristics of plasma membranes near plasmodesmata and thereby causes a permeability change which leads to leaking of electrolytes.