Purple Blotch
Disease of Onion (Allium cepa):
Perspective and Prospects
DC Manjunathagowda1,3,
R Selvakumar2, S Shilpashree3, M Anjanappa3*, R Dutta1,
MN Sharath1, SR Shalaka1, V Mahajan1
1ICAR-Directorate of Onion and Garlic Research, Rajgurunagar-410505,
Pune, Maharashtra, India
2ICAR-Indian Agricultural Research Institute, Pusa, 110012, New Delhi,
India
3College of Horticulture,
Bengaluru-560065, University of Horticultural Sciences, Karnataka, India
*For correspondence: m_anjanappa@redifmail.com
Received 12 November
2021; Accepted 30 April 2022; Published 15 June 2022
Abstract
Purple blotch
disease is a major threat to the onion crop and the disease is caused by the
pathogens Alternaria porri (Ellis) Cif. and A. allii Nolla,
thus these pathogens hamper onion cultivation across the worldwide. Hence, the
crop is protected by the spraying of chemical fungicides, thus chemicals hamper
the environment and incur additional costs to onion production and biological
agents are effective to control the pathogens under certain environmental
conditions. Hence, the development of varieties or hybrids possessing purple
blotch disease resistance is encouraged for sustainable onion cultivation.
Thus, insight into the understanding of pathogen causing purple blotch disease
is important to develop a resistant variety. The knowledge of gene action and
molecular markers linked to the resistant genes are essential for breeders for
accurate selection phenotype at early stages through indirection selection.
Thus, the available genomic sources permit for the precise mapping of resistant
genes, markers associated with the ApR1
gene would be a tool for accelerating the breeding for purple blotch disease
resistance. In view, this review confers the perspective knowledge on purple
blotch disease, causal organism, symptomatology, epidemiology, and etiology of
the pathogen, genetics of purple blotch disease resistance and breeding
prospects in onion.
Keywords: Alternaria porri (Ellis) Cif.;
Breeding; Genetics; Pathogen; Resistance
Introduction
A leaf spot
and blight disease of onion were first reported by Ajrekar (1923) from the
Bombay state of India and it was considered that disease caused by a species of
Macrosporium sp., the Macrosporium porri was first described as
blight causing pathogen of Allium species (Cooke and Ellis 1879). Thus,
the taxonomy of Alternaria species on
Allium crops causing leaf spot and
blight disease was confused, it was first described as the pathogen M. porri, later it was classified as the
taxonomy of Alternaria species by A. allii Nolla, based on the symptomatology of
pathogen (Nolla 1927), the pathogen maintains its identity with M. porri similarity, thus suggested the
appropriate name as purple blotch for the disease due to the presence of large
size lesions on leaves and seed stalks (Angell 1929) and the further name
changed to A. porri (Cifferi 1930). The name A. allii was
resurrected by Simmons (2007) in his identification manual, where it is
described as five large spored and long-beaked species from Allium, and
thus spores could distinguish based on morphology, the number of beaks and
branches, the A. porri and A. allii are closely related and form two distinct clades differ by 8
nucleotides in their RPB2 sequences (Simmons 2007; Woudenberg et al.
2014). Taxonomy of purple blotch disease-causing pathogen has been classified
in the Kingdom: Fungi, Division: Ascomycota, Class: Dothideomycetes, Order:
Pleosporales, Family: Pleosporaceae, Genus: Alternaria,
the Alternaria sect. Porri contained 82 Alternaria species, sect. Porri
of A. porri and A. allii cause purple blotch disease in onion had characterized by broadly ovoid, or obovoid, ellipsoid,
sub-cylindrical, or obclavate medium to large conidia, and were disto and
euseptate, single or in small chains with a simple or branched extended
filamentous beak. Conidia enclose multiple transverse, slightly constricted and
longitudinal septa and secondary conidiophores can form apically, or laterally
(Lawrence et al. 2013). The A.
porri isolates are unable to differentiate on conidia, conidiophores shape
and size, beak and septa of conidia. Whereas, the isolates are differentiated
based on colony color on Sabouraud's medium and Brown's medium, and were differ
significantly for aggressiveness, incubation period, disease incidence, and
disease severity. The Czapek's medium was found best for growth of isolates,
the isolates do not sporulate on culture media and sporulate poorly on the host
plant (Gupta et al. 1987).
Epidemiology of Alternia
species causing purple blotch disease
An epidemic
attack by A. porri on
onions was occurred at Baringo, Kenya occurred in the year 1961, and it causes
distinct lesions on plant leaf blades, a) purple or brown blotches (Fig. 2)
white, irregular spots or flecks with varying proportion (Bock 1964).
Sources of inoculums
Diseased
debris containing pathogen fruiting body with conidia in the farm field, or
nearby farm is the primary source of inoculum for succeeding bulb crop followed
by seed crop of onion (Pandotra 1964), fungus remain as mycelium in onion leaf
debris from diseased plants (Muimba-Kankolongo 2018) and spread by the
punctures made by the thrips, opening of stomata pores and epidermal layers.
The fruiting body with conidia of leaf lesions fabricated as principal source
of inoculum for infections and for disseminating the disease. The frequent wind
blows, and rain splashes disperse the conidia and mycelium among the stalks and
leaves of plants are the secondary source of inoculums (Fig. 1). The pathogen
prolong their existence on leaves, seed stalks and on soil surface, hence
burring of diseased debris in the soil about 2 to 6 inches deep below the soil
surface, thus lead to the complete knock out of pathogen by breaking on
existence of primary source of inoculum (Pandotra 1964, 1965).
Etiology
The conidium
germinate to form pre-penetration structure and penetrate into the leaf surface
through stomata as well as through epidermis, the maximum conidia germinate at
25°C within 24 h (h) of inoculation. The conidium produce several germ tubes
and nurture across the leaf surface, further form bulbous appressorium on
epidermal cell (52.4% of appressoria) and on stomata (48.6% of appressoria).
The bulbous primary hyphae developed under the appressoria, it could lead to
for secondary hyphae development within 48 h after inoculation, hyphae grew and
penetrate into the intercellular spaces of mesophyll cells (Aveling et al. 1994), then turned to reddish brown septate non-sporulating
mycelium (Datar 1994) and cause purple blotch lesions favored by high relative
humidity (70% RH), while low RH (40%) resulted in white flecking (often
sterile) after prolonged periods of infection. The appressoria and lesions are
form in broad optimum temperatures range from 21 to 30°C (Bock 1964).
Alternaria porri is a potentially important
pathogen in winter grown Allium
crops. The conidia of A. porri
germinate within 2 h (4°C), advances for production of terminal and intercalary
appressoria (10°C). The maximum counts of appressoria produces after 24 h at 25°C.
Pathogens penetrate via epidermis and stomata of leaves with high frequency of
stomata penetration. Prominently, infection occur after 16 h of leaf wetness at
15°C and 8 h of leaf wetness at 10–25°C, and severity of infection increases
with increasing leaf wetness over 24 h at all temperatures, and cause lesions
(Suheri and Price 2000). The moist weather causes lesions to cover with brown
mold sporangia. The suitable periods of rain, or heavy dew and favorable
environmental condition promote the disease development (Muimba-Kankolongo
2018).
Symptomatology
An epidemic
of purple blotch at Baringo, Kenya was revealed by purple or brown blotches,
and white, irregular spots or flecks with varying proportion (Bock 1964).
Symptomatic expression of purple blotch disease first appears on leaves with 2–3
mm in diameter of whitish water soaked lesions, these lesions enlarge,
coalesce, zonate and lesions turn brown to purplish color under favorable
conditions (Fig. 2). Seldom, lesion surface covered by black fruiting bodies under
humid conditions (Verma and Sharma 1999). Onion plants showing purple blotch
symptoms mainly due to the colonization of A.
porri and Stemphylium vesicarium (onion leaf blight disease),
consequently as on disease advancement the pathogens manly infect on leaves and
floral stalks shows typical purple blotch lesion symptoms, the pathogens A. porri, S. vesicarium or mixtures of both accounted for 2.6, 39.8 and
57.6%, respectively. Hence, purple blotch disease is a complex disease caused
by two pathogens by the synergistic association, S. vesicarium initiate the infection and facilitate the task of A. porri for causing purple blotch
symptoms (Abdel-Rahim et al. 2017).
The older plant tissues more susceptible than younger plants leaf blades to the
fungus infestation, infection cause small elliptic tan colored water-soaked
lesions that soon turn brownish color and later form purplish lesions with
darker margin covered by yellow zone of necrotic tissue, as on disease advances
the lesions enlarged to form concentric rings, girdling of leaf and stem cause
down fall of plant shoot (Muimba-Kankolongo 2018).
Effect of purple blotch disease incidence on plant
growth and bulb yield
Onion is susceptible to numerous foliar diseases, those
reduces bulb yield and quality (Cramer 2000) and purple blotch is an important
disease of onion across the world (Chaput 1995; Cramer 2000; Schwartz et al. 2005) especially in warm and
humid environments (Suheri and Price 2001). The fungus infestation cause on
both leaves and flower stalks (Bock 1964) and reduce onion tops production by
62–92% (Suheri and Price 2001), cause bulb yield loss of 30% (Everts and Lacy
1990) and 10% losses in s
Fig. 1: Life cycle of
Alternaria porri Cifferi causing
purple blotch disease in onion, a)
conidia mycelia present in debris, weeds and alternate host plants as act as
primary source of inoculums, b).
Diseased plants in field act as Secondary source of inoculums cause repeated
infection and lead to the disease outbreak in the crop
Fig. 2: a)
Conidium, b) Hyphae with
conidiospores and c) Purple blotch
infestion on onion crop stand
eed crop under congenial environmental
conditions (Daljeet et al. 1992;
Schwartz 2004). Purple blotch disease could cause heavy yield losses ranging
from 2.5 to 87.8 per cent during kharif
season (Srivastava et al. 1994), with
maximum percentage in Karnataka (60%) and Maharashtra (90%) states of India in kharif and rabi seasons respectively (Gupta et al. 1994). A. porri spores present in the air are
responsible for increase the disease incidence in onion crop, maximum incidence
does occur with adequate leaf wetness duration at 5°C for 16 h and 8 h at 10–25°C.
The numbers of lesions are increases with increasing leaf wetness duration and
temperature (Suheri and Price 2001). The older leaves are more susceptible than
younger leaves for purple blotch disease, infestation reduce the photosynthetic
activity of leaves, thus lead to reduction in plant growth, bulb yield and seed
yield (Verma and Sharma 1999).
Management and control of purple blotch disease – chemical
and biological agents
The losses of
bulb and seed yield of onion cause by purple blotch disease could prevent
either by protective sprays fungicides or biological agents which are antogonistic
effects on A. porri during crop
cultivation. Despite several limitations in the field conditions like frequent
or unexpected rainfall, weather modulation mainly humidity could favor to the
pathogen outbreak and thus pathogen cause severe damage on the standing crop in
the field under favorable condition. Under those circumstances the fungicide
sprays are an effective method to control the disease to maintain the crop
stand, several researchers standardized the optimum dose of sprays for the
control of disease are presented in Table 1, however it adds additional cost to
the cost of cultivation.
Table 1: Effective chemicals to control purple botch
disease under field conditions
Brand name |
Chemical composition |
Concentration |
References |
Dithane M-45 |
Mancozeb 75% WP |
0.2% |
Wanggikar et al.
(2014) |
Rovral WP |
Iprodione 41.6% |
20 g per 10 liters of water (0.2%) |
Akter et al. (2015) |
Ridomil Gold WP |
Mancozeb (64% W/W) + Metalaxyl-M (4% W/W) |
||
Dithane M-45 |
Mancozeb 75% WP |
||
AGEENT, Custom, DOZAN, Katyayani,
DuoGuard |
Cymoxanil 8% + Mancozeb 64% WP |
2500 ppm |
Rao et al.
(2015) |
Folicur |
Tebuconazole 25 EC |
0.1% |
Yadav et al.
(2017) |
Score |
Difenoconazol 25EC |
0.1% |
|
Score |
Difenconazole 25 EC |
0.1% |
Kavitha et al.
(2017) |
Nativo 75 WG |
Tebuconazole 50% + Trifloxystrobin 25% |
0.05% |
|
Roshan plus |
Hexaconazole 5% SC |
0.1% |
Nisha et al.
(2020) |
Real-mil |
Mancozeb 64%WP +Cymoxanil 8% WP |
0.3% |
The bio-control
agents are effective to control purple blotch disease, the bio agents namely Trichoderma spp., Penicillium spp., Aureobasidium pullulens, Sporobolomyces roseus and Cryptococcus luteolus were effective to control A. porri. The seed treatment with Trichoderma harzianum reduces the purple blotch disease
incidence thus increase the bulb yield of onion (Chethana et al. 2012; Mishra and Gupta 2012). The seed
treatment, seedling dip and three foliar sprays of bacteria namely Pseudomonas fluorescens, P. aeruginosa, and Bacillus subtilis, and fungi namely T. viride and T. harzianum could control the purple blotch disease in field conditions (Yadav et al. 2013). The botanical like clove extract of Allium sativum (10%) Aloe
vera (10%), neem oil (20%) and pongamia oil (20%) resulted in
inhibition of A. porri (Chethana et
al. 2012).
Development of resistance varieties to purple blotch
The
development of purple blotch disease resistant cultivars, varieties or hybrids
is another approach to control the disease, and it is an economical and
environmentally friendly method as it reduces the ecological problems caused by
the use chemicals to control purple blotch disease. However, the fungicides
available in the market have low potential to manage onion purple blotch
disease (Uddin et al. 2006;
Abdel-Hafez et al. 2014). In this
context, there is a need of hunting resistance source for purple blotch disease
to improve the bulb production and productivity. Thus, at present there were no
potential onion varieties or hybrids succeed in onion acreage showing
resistance to purple blotch disease. Nevertheless, several researchers are
hunting for purple blotch disease resistance source of resistance lines from
past several years.
The
onion hybrids cross viz., Red Creole
× Kaharda and Kaharda × Red Creole were resistant to purple blotch disease, these
hybrids are performed better than their parents and other hybrids in terms of
disease incidence and bulb yields, negative environmental correlation was noted
between disease incidence and bulb yield significantly, higher disease incidence could lower bulb
yield was due to environmental effects rather than the genotypes (Abubakar and
Ado 2008).
Selves
of second-generation mutant (M2) onion plants under epiphytotic
conditions, revealed the disease resistance against purple blotch with 7.60% M2
plants (1–10 PDI), while 12.80% M2 plants with moderately resistance
(11–25 PDI), these disease resistance plants was associated with more than two
times higher chlorophyll content (95.8–108.10 mg/100 g) with dark waxy leaves
than the normal green foliage (Patil et
al. 2008). The disease resistance (1–10 PDI) was noticed in M4
white onions (15.80%) than the M4 red onions (2.20%). Furthermore,
majority of M4 population (about 70–75%) were moderate resistance
(11–25 PDI) against the purple blotch disease in both red and white onions.
Therefore, further crop improvement is essential for incorporation of disease
resistance by advancement of 3–4 selection cycles (Patil et al. 2009).
Purple
blotch disease resistance attributed by cuticle thickness; thus resistance
could break by wounding and it is naturally associated with sand storm blast
(Bock 1964). The cultivars screened in search of resistance to purple blotch
disease, thus the varieties VL-1, PBR-1, PBR-5 and PRR are found resistant to
purple blotch disease (Daljeet et al.
1992). The onion accession
CBT-Ac77 and the variety Arka Kalyan was found highly resistant to purple
blotch resistance among 43 Allium
genotypes screened under field conditions, thus suggested the newly identified
resistance sources were the potential donors for purple blotch resistance
breeding (Nanda et al. 2016).
Genetics of purple blotch resistance
The purple
blotch disease resistance line PBR-287 was identified as a good source of
resistance, and hence it was used in the cross with susceptible parent.
Parents, F1 and individual F2 progenies were subjected
for genetics of resistance and RAPD marker analysis. The results reveal that F2
individuals segregated in 3:1 ratio for resistance (Ganesh and Veeregowda 2005).
The molecular markers linked to purple blotch disease resistance was developed
by using F1, F2, and BC1 populations, which
were developed from resistant (R) parent Arka Kalyan and the susceptible (S)
parent Agrifound Rose. The inheritance of purple blotch disease revealed that
the F1 was resistant, while 498 F2 plants and 128 BC1
lines segregated in 3R:1S and 1R:1S ratio. Hence, A. porri resistance (ApR)
is controlled by a single dominant gene and thus designated as ApR1 gene (Chand et al. 2018).
Molecular perspective
Three
breeding lines PBR-287, MS-65-268 and Arka Kalyan-704 were identified as
resistant to purple blotch disease, and these lines were subjected to random
amplified polymorphic DNA (RAPD) analysis with 160 ten mer random primers for
identification and estimation of genetic relationship among resistant and
susceptible (Arka Niketan) varieties. Out of 160 primers 41 primers are
exhibited polymorphism among the accessions, and DNA profile with 5 primers
namely OPB02, OPB13, OPC09, OPC12 and OPF08 distinguished resistant lines from
the susceptible line. The PCR products ranged from 300 bp to 2000 bp and were
consistent, unambiguous and repeatable primer with an average of 2.65
polymorphic bands, 11.65 monomorphic bands were produced per primer (14.3
bands). Principle component analysis (PCA) confirmed the least genetic
dissimilarity (40%) was recorded between PBR-287 and MS-65-268; whereas, the
highest (65%) was found between lines Arka
Niketan-709 and MS-65-268 (Ganesh and Veeregowda 2005). The nucleotide rbcL and matK were used and developed SSR markers to detect the purple leaf
blotch (PLB) gene, and it does exist
on shorter arm of eight chromosome at s1/s2 locus.
The PLB gene conferred resistance to
purple leaf blotch in onion mutant lines
(BP2-75/2, BP2 -100/1, BP2-100/2) and mutant variety BARI Piaz-2 was
successfully detected in the mutant lines using SSR markers (Chakraborty et al. 2015). The ApR1 gene was
linked with seven markers namely AcISSR471257, AcISSR681600,
AcISSR1031416, AcSSR7, AcSSR22, AcSSR31, and AcSSR33 showed
polymorphism among resistant and susceptible bulks and were used in genotyping
of mapping populations (F2 and BC1). The three inter
simple sequence repeats (ISSR) were converted into sequence-tagged markers
(STS), the single-copy status of resistant locus association confirmed by
southern blotting. The markers linked closely at 1.3 centi Morgan (cM) distance
of AcSSR7 (SSR) and ApR-450 at 1.1 cM (STS) to the ApR1 locus. These
findings could be recommended for facilitating the introgression of ApR1
gene to desirable genotypic backgrounds (Chand et al. 2018).
Conclusion and Future Perspective
Purple blotch caused by A. porri is a serious disease, incur to
heavy yield losses in the bulb and seed crop of onion. The yield losses can be
controlled by efficient crop management practices, crop rotation, protective
sprays with fungicides, use of biological agents in onion production could
control the purple blotch disease, but these crop management activates add the
additional cost to the production cost of onions. Thus, the identification of
effective and stable resistance varieties are Arka Kalyan, VL Paiz-1
and breeding lines PBR-287,
PBR-1, PBR-5 and PRR (Ganesh and Veeregowda 2005; Daljeet et al. 1992),
hybrids are Red Creole × Kaharda and Kaharda × Red Creole (Abubakar and Ado
2008), accession namely CBT-Ac77 (Nanda et
al. 2016) would be useful sources of resistance to purple blotch thus these
are useful in breeding of onions resistance to purple blotch. Development
of genomic SSR markers is a practical tool set for genetics studies in onion
(Baldwin et al. 2012), thus ApR1 gene flanking markers could be
applicable in MAS with high efficiency (Chand et al. 2018). The chromosomal location of the ApR1 gene is yet to be ascertain, thus fine mapping of resistant
locus may be preceded by advanced DNA markers such as single nucleotide
polymorphisms (SNPs) with more close linkage (Chand et al. 2018). The validation of ApR1
gene flanking SSR and ISSR markers in other genotypes need to be focused
for the identification and isolation of potential purple blotch disease
resistance source.
Conflict of Interest
We the authors declare that have no conflict of
interest.
Ethical Approvals
The manuscript was not
submitted anywhere else, and results were presented without fabrication,
falsification, or inappropriate data manipulation. Research does not pose any
threat to public health or national security.
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