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Indian Phytopathology

, Volume 71, Issue 1, pp 91–102 | Cite as

Risk of pathogens associated with plant germplasm imported into India from various countries

  • Baleshwar Singh
  • Jameel Akhtar
  • Aravindaram Kandan
  • Pardeep Kumar
  • Dinesh Chand
  • Ashok Kumar Maurya
  • Prakash Chand Agarwal
  • Sunil Chandra Dubey
RESEARCH ARTICLE
  • 67 Downloads

Abstract

During 2012–2014, a total of 309,182 germplasm samples including trial materials were received in the form of seeds, vegetative propagules and in vitro plantlets from different countries. These samples were tested for quarantine clearance resulted in interception of 30 pathogenic fungi and one bacterium in 63 crop species from 35 countries including Peronospora manshurica and Fusarium oxysporum f. sp. cucumerinum (not reported from India); Bipolaris maydis, B. oryzae, Colletotrichum gloeosporioides, C. lindemuthianum, Fusarium solani, F. verticillioides, Puccinia carthami (have different races); Botrytis cinerea, Phoma sorghina, Rhizoctonia solani, Macrophomina phaseolina, Sclerotinia sclerotiorum (have wide host range); Tilletia barclayana (have limited distribution); Alternaria ricini on Tagetes spp., Bipolaris maydis on Capsicum annuum, B. oryzae on Brassica oleracea var. botrytis and Solanum lycopersicum and Colletotrichum capsici on Abelmoschus esculentus (new host record), etc. and Xanthomonas campestris pv. campestris (have different races) which are of quarantine significance to India. Infected samples were salvaged by adopting suitable techniques, however, 636 samples could not be salvaged, hence, rejected and incinerated. Interception of large number of pathogens of quarantine significance on a wide range of crops from different countries emphasizes the need for utmost care and vigilance during quarantine processing of imported plant genetic resources to biosecure India by intercepting the entry of exotic pathogens or more virulent races/strains in the country.

Keywords

Import Germplasm Interception Quarantine Salvaging 

Introduction

International exchange of plant genetic resources (PGR) has a significant role in crop improvement programmes for food security. However, exchange of PGR has an inherent risk of inadvertent introduction of exotic pests or their more virulent strains/races into new geographical areas. In India, ICAR-National Bureau of Plant Genetic Resources (ICAR-NBPGR), New Delhi, is the nodal agency for quarantine processing of introduced germplasm including transgenics for research purposes. A number of pathogens of high economic importance have been intercepted from time to time during quarantine processing (Dev et al. 2012; Singh et al. 2014, 2015). Therefore, plant quarantine, as a biosecurity tool, assumes special importance in order to prevent the entry of exotic pests, including fungi and bacteria, while introducing PGR into the country. The pathogens intercepted in introduced PGR during 2012–2014 are listed here and discussed their quarantine significance.

Materials and methods

During 2012–2014, a total of 309,182 germplasm samples including trial material were received in the form of seeds, vegetative propagules including stem cuttings, rooted plants, bulbs, tubers and in vitro plantlets from different countries and processed under quarantine. All the samples were first examined visually and then under a stereo-binocular microscope for the presence of fungal fructifications such as ergot sclerotia, rust/smut spores, pustules, bunt balls and for symptoms such as discolourations, deformation, malformation etc. Seeds suspected to be contaminated with oospores/spores of rust/smut/mildews were subjected to washing test and the supernatant was examined under the stereo-binocular microscope and compound microscope for detection of oospores/spores (Dev et al. 2012).

Unhealthy-looking seeds/plant parts of all the samples were subjected to blotter test. The seeds were placed on three layers of moist blotting papers in plastic Petri plates. The number of seeds per plate varied from 10 to 25, depending on the size of both the seed and sample and incubated at 22 ± 1 °C for 7 days under alternating cycles of 12 h light and darkness and examined on 8th day for growth of fungi and bacteria. Pathogenic fungi were identified on the basis of colony characters/fruiting bodies under stereo-binocular microscope and spore characters under compound microscope as per the characteristics described by Mathur and Kongsdal (2003) and IMI descriptions of fungi and bacteria.

Brassicas seedlings showing ‘V’ shaped lesions in the blotter test were cut with a sharp sterilized blade, mounted in water drop and examined under compound microscope. A slow to fast oozing of bacterium from vascular bundles indicated the bacterial association with infected portion (Singh et al. 2006). The bacterium was isolated on nutrient-agar medium and examined after 72 h of incubation. Studies on morphological, cultural and biochemical characteristics were undertaken to identify the bacterium (Schaad et al. 2001).

The infected/contaminated seeds and vegetative propagules were salvaged by using various suitable techniques viz., mechanical separation, hot water treatment (HWT), ethyl alcohol wash, fungicidal seed dressing/spray, etc. (Singh and Khetarpal 2005). The samples which could not be salvaged were rejected and incinerated.

Results and discussion

The quarantine processing of imported germplasm samples resulted in the interception of 30 fungal pathogens and one phytopathogenic bacterium in 63 crop species from 35 countries as listed in Table 1.
Table 1

Pathogenic fungi and a bacterium intercepted in introduced germplasm during 2012–2014

Fungi/bacterium

Host

Country/source

Infection (%)

Alternaria brassicae d,g,i

B. juncea

Canada (1/350)a

0.29

B. oleracea var. capitata

The Netherlands (2/77)

2.60

B. rapa

Canada (1/86)

1.16

A. brassicicola d,i

B. carinata

Canada (21/91)

23.08

B. juncea

Canada (6/350)

1.71

B. nigra

Canada (1/21)

4.76

B. o. var. botrytis

The Netherlands (5/218)

2.29

B. o. var. capitata

The Netherlands (12/85)

14.12

B. rapa

Canada (6/86)

6.98

Brassica spp.

UK (1/2816)

0.04

A. padwickii d,i

O. sativa

Brazil (1/75)

1.33

  

China (2/70)

2.86

  

Germany (1/2)

50.00

  

Nepal (3/36)

8.33

  

Philippines (10/1069)

0.94

A. ricini d,i

Tagetus spp.f

USA (1/66)

1.52

Ascochyta pisi d,i

L. sativus

Syria (12/503)

2.39

Bipolaris maydis d,g,i

C. annuum f

Korea (2/102)

1.96

 

Z. mays

Brazil (2/86),

2.33

  

Mexico (1/2)

50.00

  

Philippines (1/27)

3.70

  

Thailand (9/1903)

0.47

  

USA (1/6)

16.67

B. oryzae d,g,i

B. o. var. botrytis

The Netherlands (1/103)

0.97

S. lycopersicum f

USA (1/47)

2.13

O. sativa

Brazil (7/81)

8.64

China (3/144)

2.08

Columbia (2/38)

5.26

France (1/2)

50.00

Nepal (1/36)

2.78

Philippines (1/86)

1.16

USA (6/286)

2.10

B. sorokiniana d,i

S. lycopersicum

Thailand (1/29)

3.45

  

USA (1/47)

2.13

T. aestivum

Australia (15/2033)

0.74

 

Mexico (1/117)

0.85

  

USA (5/146)

3.42

 

T. monococcum

USA (3/150)

2.00

Botrytis cinerea d,g,i

A. cepa

UK (1/80)

1.25

B. o. var. botrytis

Netherlands (1/170)

0.59

C. annuum

Taiwan (1/5)

20.00

Carthamus spp.

Germany (2/32)

6.25

S. trifoliatum

Czech Republic (1/8)

12.50

Colletotrichum capsici d,g,i

A. esculentus f

Taiwan (2/224)

0.89

C. annuum

Taiwan (1/81)

1.23

 

USA (1/199)

0.50

G. max

Japan (4/14)

28.57

Tagetus spp.

USA (1/66)

1.52

C. gloeosporioides d,g,i

C. annuum

Taiwan (3/81)

3.70

C. lindemuthianum d,g,i

G. max

Costa Rica (1/59)

1.69

Diplodia macrospora d

Z. mays

Thailand (2/791)

0.25

Fusarium oxysporum d,i

A. fistulosum

Japan (1/93)

1.08

C. moschata

USA (2/93)

2.15

O. ficus-indica

Italy (1/165)

0.61

S. lycopersicum

Taiwan (1/18)

5.56

T. aestivum

UK (2/194)

1.03

V. mungo

USA (1/30)

3.33

Z. mays

Brazil (2/56)

3.57

Mexico (1/1)

100.00

F. o. f. sp. cucumerinumd,e

C. melo

USA (1/12)

8.33

F. solani d,g,h,i

C. annuum

France (2/242)

0.83

 

Korea (1/231)

0.43

 

Taiwan (8/176)

4.55

 

USA (1/199)

0.50

Capsicum spp.

USA (3/232)

1.29

Cucumis spp.

USA (1/18)

5.56

Cucurbita moschata

USA (1/93)

1.08

G. max

Colombia (1/60)

1.67

 

Costa Rica (17/59)

28.81

L. aegyptica

USA (1/21)

4.76

M. indica

Israel (37/2742)

1.35

M. charantia

Thailand (1/6)

16.67

O. ficus-indica

Italy (3/165)

1.82

O. vulgare

USA (1/15)

6.67

O. sativa

USA (3/159)

1.87

P. glaucum

USA (2/22)

9.09

S. lycopersicum

Netherlands (2/17),

11.76

 

Taiwan (1/13),

7.69

 

USA (3/236)

1.27

Solanum spp.

Spain (1/4)

25.00

 

Taiwan (2/176)

1.14

V. sativa

USA (1/5)

20.00

Z. mays

Brazil (4/45)

8.89

Chile (1/5247)

0.02

Mexico (3/209)

1.44

Thailand (6/2044)

0.29

USA (9/452)

1.99

F. verticillioides d,g,h,i

A. esculentus

Taiwan (16/63)

25.40

A. porrum

USA (1/4)

25.00

A. tuberosum

USA (1/4)

25.00

Amaranthus tricolor

Taiwan (1/33)

3.03

Basella alba

Taiwan (2/10)

20.00

Benincasa hispida

Thailand (1/33)

3.03

B. carinata

Canada (2/91)

2.20

B. juncea

Canada (3/550)

0.55

B. o. var. botrytis

Netherlands (8/369)

2.17

B. o. var. capitata

Netherlands (1/77)

1.33

B. rapa

Canada (2/86)

2.33

Brassica spp.

UK (6/4419)

0.14

C. annuum

France (1/242)

0.41

 

Guatemala (7/16)

43.75

 

Korea (3/141)

2.13

 

Netherlands (4/212)

1.89

 

Taiwan (8/147)

5.44

 

USA (19/938)

2.03

Capsicum spp.

USA (5/232)

2.16

Carthamus spp.

Germany (1/32)

3.13

Chamaecytisus palmensis

Australia (1/1)

100.00

C. arietinum

USA (2/19)

10.53

Citrullus lanatus

USA (5/244)

2.05

Citrullus spp.

USA (4/92)

4.35

C. melo

Netherlands (1/130)

0.77

 

USA (4/42)

9.52

C. sativus

Netherlands (1/231)

0.43

 

Taiwan (3/28)

10.71

Cucumis spp.

USA (2/18)

11.11

C. moschata

Taiwan (1/6)

16.67

Cucurbita spp.

USA (1/6)

16.67

Dianthus sp.

USA (2/503)

0.40

Dolichos lablab

Taiwan (6/35)

17.14

G. max

Brazil (1/1)

100.00

 

Colombia (15/60)

25.00

 

Costa Rica (40/59)

67.80

 

Japan (2/36)

5.56

Gossypium austral

Australia (1/2)

50.00

G. barbadense

Israel (1/5)

20.00

G. hirsutum

USA (21/76)

27.63

Hippophae rhamnoides

Russia (2/5)

40.00

Lagneria siceraria

Netherlands (1/2)

50.00

 

USA (3/41)

7.32

L. acutangula

Taiwan (2/6)

33.33

L. aegyptica

Taiwan (1/14)

7.14

 

USA (5/25)

20.00

S. lycopersicum

USA (10/298)

3.36

M. indica

Israel (55/2742)

2.01

Melilotus spp.

USA (3/837)

0.36

M. charantia

China (1/5)

20.00

 

Thailand (2/15)

13.33

O. vulgare

USA (1/15)

6.67

O. sativa

Belgium (1/1)

100.00

 

Brazil (5/304)

1.64

 

China (7/144)

4.86

 

France (2/2)

100.00

 

Germany (2/2)

100.00

 

Nepal (3/36)

8.33

 

Philippines (25/1486)

1.68

 

USA (32/648)

4.94

P. glaucum

USA (10/22)

45.45

Phaseolus vulgaris

USA (2/364)

0.55

S, lycopersicum

France (1/186)

0.54

 

Guatemala (1/2)

50.00

 

The Netherlands (4/88)

4.55

 

Taiwan (17/124)

13.71

 

Thailand (5/80)

6.25

 

USA (15/356)

4.21

S. melongena

Taiwan (4/119)

3.36

Solanum spp.

Spain (3/4)

75.0

 

Taiwan (1/19)

5.26

Sorghum bicolor

Ethiopia (1/19)

5.26

 

Japan (30/404)

7.43

Tagetus spp.

USA (2/66)

3.03

Trigonella spp.

USA (1/41)

2.44

T. aestivum

Australia (6/2033)

0.30

 

South Africa (2/65)

3.08

 

UK (5/194)

2.58

 

USA (4/117)

3.42

T. monococcum

USA (3/150)

2.00

V. ungiculata

Taiwan (8/30)

26.67

Z. mays

Brazil (36/394)

9.14

  

Chile (83/5247),

1.58

  

China (1/8),

12.5

  

Mexico (77/1154),

6.67

  

Philippines (8/112),

7.14

  

Switzerland (3/30),

10.00

  

Thailand (118/4419)

2.67

  

USA (76/2650)

2.87

Macrophomina phaseolina d,h,i

A. esculentus

Bangladesh (1/5)

20.00

G. max

Japan (1/14)

7.14

M. indica

Israel (1/728)

0.14

M. charantia

Thailand (1/6)

16.67

S. bicolor

Chile (2/5247)

0.04

Melanospora zamiae d

Z. mays

Chile (1/5247)

0.02

  

Thailand (1/40)

2.50

  

USA (27/474)

5.70

Peronospora manshurica b,c,e,g

G. max

Canada (10/100)

10.00

  

Colombia (2/60)

3.33

  

Japan (1/14)

7.14

  

Taiwan (3/100)

3.00

Phoma exigua var. exiguad

C. annuum

Taiwan (2/81)

2.47

Cucurbita spp.

USA (1/6)

16.67

G. hirsutum

Japan (2/42)

4.76

O. sativa

Brazil (1/298),

0.34

 

USA (1/4)

25.00

M. charantia

Thailand (7/34)

20.59

P. lingam d

B. napus

Australia (1/20)

5.00

B. rapa

Canada (1/86)

1.16

P. sorghina d,g,h

B. o. var. botrytis

Netherlands (2/96)

2.08

B. rapa

Canada (1/86)

1.16

Brassica spp.

UK (2/2816)

0.07

C. annuum

Taiwan (6/81)

7.41

 

USA (1/85)

1.18

Carthamus spp.

USA (2/61)

3.28

C. lanatus

USA (2/197)

1.02

Citrullus spp.

USA (2/92)

2.17

Citrullus var. citroides

USA (1/1)

100.00

C. melo

Japan (2/13)

15.38

 

Thailand (1/10)

10.00

C. sativus

Bangladesh (2/6)

33.33

C. moschata

USA (1/93)

1.08

L. siceraria

USA (4/41)

9.76

L. acutangula

USA (3/4)

75.00

L. aegyptica

USA (1/21)

4.76

Melilotus spp.

USA (1/837)

0.12

O. ficus-indica

Italy (1/165)

0.61

O. sativa

Brazil (4/81)

4.94

 

Germany (2/2)

100.00

 

Philippines (4/171)

2.34

 

USA (2/35)

5.71

P. glaucum

USA (2/22)

9.09

S. lycopersicum

France (1/11)

9.09

 

USA (1/33)

3.03

S. melongena

France Taiwan (8/106)

7.55

Solanum spp.

Spain (1/4)

25.00

S. bicolor

Ethiopia (3/5247)

0.06

T. aestivum

Kenya (1/1)

100.00

V. mungo

USA (1/30)

3.33

Z. mays

Mexico (1/2)

50.00

  

Thailand (2/1458)

0.14

Puccinia carthami b,c,g

Carthamus tinctorius

USA (207/207)

100.00

Carthamus spp.

Germany (4/32),

12.50

  

USA (33/61)

54.10

Rhizoctonia solani d,i,g

L. acutangula

USA (1/4)

25.00

O. sativa

Brazil (1/6),

16.67

 

Philippines (1/86)

1.16

Z. mays

Chile (1/5247)

0.02

Sclerotinia sclerotiorum d,g,i

C. annuum

USA (1/18)

5.56

L. siceraria

USA (1/37)

2.70

S. bicolor

Japan (5/404)

1.24

Tilletia barclayana b,i

O. sativa

Brazil (1/51)

1.96

  

China (306/1021)

29.97

  

Nepal (2/36)

5.56

  

Philippines (2/80)

2.50

  

USA (88/584)

15.07

  

Vietnam (50/74)

67.57

T. foetida b,i

T. aestivum

Lebanon (5/845)

0.59

Ustilaginoidea virens b,i

O. sativa

Brazil (2/75)

2.67

  

China (11/215)

5.12

  

Columbia (4/38)

10.53

  

Nepal (13/641)

2.03

  

Philippines (24/787)

3.05

  

USA(1/76)

1.32

  

Vietnam(1/28)

3.57

Verticillium albo-atrumd,g,h

A. esculentus

Taiwan(1/24)

4.17

B. o. var. botrytis

Netherlands (12/273)

4.40

Carthamus spp.

Germany (2/32)

6.25

Dianthus spp.

USA (1/503)

0.20

O. sativa

USA (1/83)

1.20

Xanthomonas campestris pv. campestrisd,g,i

B. carinata

Canada (2/91)

2.20

 

B. o. var. botrytis

Netherlands (3/199)

1.51

 

B. o. var. capitata

Netherlands (1/5)

20.00

 

B. juncea

Canada (1/350)

0.29

 

B. rapa

Canada (2/86)

2.33

aFigures in parentheses are number of infected samples/total number of samples; Seed health testing method used: bvisual examination; cwashing test; dincubation test; Pathogens: epathogen not yet reported from India, fpathogen not yet reported on the host, gphysiological races of pathogen reported, hpathogen has broad host range, ipathogen causing significant economic losses

Visual/stereoscopic observations and seed washing test revealed presence of Peronospora manshurica (Naumov) Syd. ex Gaum. the causal agent of downy mildew of soybean in Glycine max from Canada (10.00%), Colombia (3.33%), Japan (7.14) and Taiwan (3.00%). P. manshurica is yet not reported from India, however, it has been repeatedly intercepted on soybean seeds from several countries including Malaysia and Indonesia, the countries where it has not been reported. Oospore of P. manshurica can remain viable for eight years and the fungus is reported to have a large number of physiological races (Agarwal et al. 2006). All the infected samples were rejected and incinerated.

Puccinia carthami Corda (rust of safflower) was intercepted on Carthamus tinctorius from USA (100.00%); in Carthamus spp. from Germany (12.50%) and USA (54.10%). P. carthami has a number of races which differ in ability to attack certain safflower varieties/lines (https://archive.org/stream/safflowerdisease3452thom/safflowerdisease3452thom_djvu.txt). The infected/contaminated seed were removed mechanically followed by ethyl alcohol wash and drying (Dev et al. 2012). Tilletia barclayana (Bref.) Sacc. & Syd. (Syn: Neovossia horrida (Takah.) Padwick & Khan), the causal agent of smut, bunt of rice was intercepted in O. sativa from Brazil (1.96%), China (29.97%), Nepal (5.56%), Philippines (2.50%), USA (15.07%) and Vietnam (67.57%).

Yield losses as high as 15% have been reported due to T. barclayana (Webster and Gunnell 1992). The International Rice Research Institute reported that it is a seed-borne pathogen of quarantine importance.

Tilletia foetida (Wallr.) Liro (Syn. Tilletia laevis Kühn), causing hill bunt, common bunt and stinking smut of wheat was intercepted on Triticum aestivum from Lebanon (0.59%). Although the disease causes little yield loss, however, Nagy and Moldovan (2006) reported that if untreated seeds were sown, the incidence of common bunt could reach up to 70–80%, causing yield losses up to 40% in Romanian conditions. The infected/contaminated seed were removed mechanically followed by ethyl alcohol wash and drying (Dev et al. 2012).

Ustilaginoidea virens (Cke.) Tak. (Syn. Claviceps oryzae-sativae Hashioka), causal agent of false smut/green smut of rice, was intercepted on O. sativa from Brazil (2.67%), China (5.12%), Columbia (10.53%), Nepal (2.03%), Philippines (3.05%), USA (1.32%) and Vietnam (3.57%). Upadhyay and Singh (2013) reported yield losses due to false smut in rice ranging from 4.3 to 20.0%. The infected/contaminated seed were removed mechanically followed by ethyl alcohol wash and drying (Dev et al. 2012).

Observations on seeds/other planting material incubated on moist blotters resulted in the interception of 25 seed-borne fungi and one bacterium of economic significance (Table 1). Some of the important pathogens are discussed below:

Alternaria brassicae (Berk.) Sacc., causal agent of Altenaria blight, leaf blight fungus of crucifers was intercepted in Brassica juncea (0.29%), in B. rapa (1.16%) from Canada and in B. oleracea var. capitata from The Netherlands (2.60%). Alternaria brassicicola (Schwein.) Wiltshire, the causal agent of Alternaria blight, black spot of crucifers and brown rot of cabbage was intercepted in a number of brassicas from several countries (Table 1). Prasad and Vishunavat (2006) reported maximum loss (49.97%) in seed test weight in cauliflower seed crop due to Alternaria blight (A. brassicae and/or A. brassicicola). Hossain and Mian (2005) reported seed yield loss of 59% in cabbage due to Alternara blight (A. brassicicola) in Bangladesh.

Alternaria ricini (Yosh & Toki) Hansf. (Syn. Macrosporium ricini Yoshii) causal agent of leaf spot and seedling blight in castor bean was intercepted in Tagetus spp. from USA (1.52%). It was reported that about 70% plants to be affected with the Alternaria blight disease caused serious losses in yield and oil content in castor (http://www.ikisan.com/tg-castor-disease-management.html#AlternariaBlight). Interception of A. ricini in Tagetus spp. is a new host record.

Bipolaris maydis (Nisik. & Miyake) Shoem [anamorph] (syn. Drechslera maydis (Nisikado & Miyabe) Subram. & Jain) [= Cochliobolus heterostrophus (Drechsler) Drechsler] a Maydis leaf blight, Southern leaf blight of maize fungus was intercepted in Capsicum annuum from Korea (1.96%); in Zea mays from Brazil (2.33%), Mexico (50.00%), Philippines (3.70%), Thailand (0.47%) and USA (16.67%). Sharma and Rai (2000) reported 41% crop losses in productivity due to Maydis leaf blight in India. Interception of B. maydis on C. annuum is a new host record.

Bipolaris oryzae (Breda de Haan) Shoemaker (syn. Drechslera oryzae (van Breda de Haan) Subram. & Jain, [= Cochliobolus miyabeanus (Ito & Kurib.) Drechsler ex Dastur], the causal organism of brown leaf spot disease of rice, was intercepted in Brassica oleracea var. botrytis from The Netherlands (0.97%); in Solanum lycopersicum from USA (2.13%); in O. sativa seeds from Brazil (8.64%), China (2.08%), Columbia (5.26%), France (50.00%), Nepal (2.78%), Philippines (1.16%), USA (2.10%). B. oryzae has been known to cause considerable yield losses in rice. In India brown leaf spot disease was the main cause of the Great Bengal Famine of 1943 which resulted in significant yield losses (Padmanabhan 1973). B. o. var. botrytis and S. lycopersicum are the new host records for B. oryzae.

Botrytis cinerea Pers.: Fr [anamorph] (= Botryotinia fuckeliana (de Bary) Whetzel [teleomorph] causes botrytis rot, grey mould diseases in a very wide range of plants was intercepted in Allium cepa from UK (1.25%), in B. o. var. botrytis from The Netherlands (0.59%); in C. annuum from Taiwan (20.00%), in Carthamus spp. from Germany (in 6.25%), in Silphium trifoliatum from Czech Republic (12.50%). Weiberg et al. (2013) reported that B. cinerea infects almost all vegetable and fruit crops and caused annual losses of US $ 10–100 billion worldwide.

Colletotrichum capsici (Syd.) Butler & Bisby (syn. Colletotrichum dematium (Pers.) Grove), causing leaf spot, anthracnose and fruit rot in peppers, was intercepted in Abelmochus esculentus from Taiwan (0.89%), in C. annuum from Taiwan (1.23%), USA (0.50%), in Glycine max from Japan (28.57%) and in Tagetus spp. from USA (1.52%) (Table 1). This fungus has 45 major, minor and wild hosts and has been intercepted in India on several other hosts in the past from different countries (Singh et al. 2005; Agarwal et al. 2007). Colletotrichum gloeosporioides (Penz.) Sacc. [= Glomerella cingulata (Stonem.) Spauld. & Schrenk] a causal agent of anthracnose, fruit rot was intercepted in C. annuum from Taiwan (3.70%). The estimated loss due to anthracnose ranged from 8 to 60% in different parts of India (Raj and Christopher, 2009). Sharma et al. (2011) reported the existence of 19 races in C. capsici and six races in C. gloeosporioides associated with fruit rot complex while screening the germplasm of Capsicum. C. capsici is not yet reported in A. esculentus, therefore, interception of C. capsici on A. esculentus is a new host record.

Colletotrichum lindemuthianum (Sacc. & Magnus) Briosi & Cavara causing anthracnose in legumes was intercepted in 1.69% samples of G. max from Costa Rica. Sharma et al. (2008) reported that under favourable conditions anthracnose infection can lead to an epidemic which may result in 100% yield losses in kidney bean. The fungus is known to have races that vary from country, region, location, and variety and over 100 races have been characterized worldwide (Padder et al. 2010).

Diplodia macrospora Earle (Syn. Stenocarpella macrospora (Earle) Sutton) causing dry rot disease of ears and stalks in maize was intercepted in 0.25% samples of Z. mays from Thailand. In India, the disease is restricted to Sikkim region only (CAB International 2007). Losses due to stalk and grain rots vary from season to season and between regions, but may be greater than 50% and yield reductions of 10-20% are common in the USA (CABI 2007). S. macrospora and S. maydis are A2 quarantine organisms for EPPO (OEPP/EPPO 1982).

Fusarium oxysporum f. sp. cucumerinum Owen (Syn. Fusarium cucumerinum Berk & Broome) causal agent of Fusarium wilt of cucumber was intercepted in 8.33% samples of Cucumis melo from USA. It is economically important wilt pathogen of cucumber and causing significant yield losses in greenhouse cucumber. Since this fungus is yet not known to occur in the country, its interception is of quarantine significance to India. Therefore, the infected sample was rejected and incinerated.

Fusarium solani (Martius) Sacc. causes wilt and damping-off disease on a number of crop species, was intercepted on many crops from different countries (Table 1). F. solani has been repeatedly intercepted on more than 60 crop species from several countries during quarantine processing (Agarwal et al. 2001). It causes substantial economic losses worldwide and molecular studies revealed high level of diversity within the fungal population.

Fusarium verticillioides (Sacc.) Nirenberg (syn. F. moniliforme Sheldon), the causal organism of bakane/stalk/stem/ear rot diseases, was intercepted in several crops from various countries (Table 1). This fungus is reported to have genetic variability (Sharma et al. 2014). Hossain et al. (2013) also reported 51.53 and 37.60% yield reduction in infected hill of Aus and Aman rice varieties, respectively from Bangladesh.

Macrophomina phaseolina (Tassi) Goid (Syn.- Rhizoctonia bataticola (Taubenh.) Butler; Sclerotium bataticola Taubenh.), the causal agent of charcoal rot, ashy stem blight and root rot in a variety of crops, was intercepted in Abelmoschus esculentus from Bangladesh (20.00%); in Glycine max from Japan (7.14%); in Mangifera indica from Israel (0.14%); in Momordica charantia from Thailand (16.67%) and in Sorghum bicolor from Chile (0.04%). Yield losses due to this fungus have been reported in sunflower (36.8-79.2%) from Venezuela and in sorghum (31-38%) from India (CAB International 2007).

Melanospora zamiae Corda, the causal agent of crown rust of maize was intercepted in Z. mays from Chile (0.02%), Thailand (2.50%) and USA (5.70%). The report of the Technical Working Group 1 of Australia listed this as a pathogen of quarantine significance and highlighted the risk associated in the bulk maize import from USA (Irwin et al. 1999).

Phoma lingam (Tode ex Fr) Desm. [= Leptosphaeria maculans (Desm.) Ces. & De Not.] the causal agent of black leg in crucifers was intercepted in Brassica rapa from Canada (1.16%) and in B. napus from Australia (5.00%). Hammoudi et al. (2012) reported yield losses up to 95% due to black leg in oilseed rape.

Verticillium albo-atrum Reinke & Berthold causes Verticillium wilt disease in several crops, was intercepted in A. esculentus from Taiwan (4.17%), in B. o. var. botrytis from The Netherlands (4.40%); in Carthamus spp. from Germany (6.25%); in Dianthus spp. from USA (0.20%) and in O. sativa (1.20%). A yield loss of 10–25% has been reported in hydrophonics and soil-grown rockwool crops (Horticultural Development Council 2007).

Some other fungi intercepted were Acremonium strictum Gams (Syn. Cephalosporium acremonium) in A. esculen tus from Taiwan; in B. o var. botrytis from The Netherlands; in C. annuum from USA, in G. max from Costa Rica, in T. aestivum from USA; Ascochyta pinodes Jones in C. annuum from Taiwan; Bipolaris halodes in O. sativa from USA; B. rostrata in C. annuum from Korea; B. sacchari (Butler) Shoemaker in Lolium rigidium from USA; B. tetramera in C. annuum from Guatemala and Taiwan, in S. lycopersicum from USA, in Vigna mungo from USA; Cephalosporium maydis Samra, Sabet & Hingorani in B. juncea from Canada, in C. annuum from Guatemala, in Cicer arietinum, Hordeum vulgare, Trigonella spp. and Z. mays from USA; Corynespora cassicola in Lathyrus sativus from Lebanon; F. culmorum in Opuntia ficus-indica from Italy; F. dimerum in O. sativa from Brazil and USA; F. equiseti in A. fistulosum from Japan; F. semitectum in Aegilops tauschii, Melilotus spp., S. lycopersicum and T. aestivum from USA, in B. juncea from Canada, in C. annuum from Korea and Guatemala, in Oryza sativa from Philippines, The Netherlands, in Z. mays from Thailand and USA; Myrothecium verrucaria in Cucurbita spp. from USA; Nigrospora oryzae in C. annuum from Philippines, USA; in Momordica charantia from Thailand, in O. sativa from Philippines, USA; Pestalotia juepini in Leucodendron safari from sunset Australia; Phoma leveillei in Chamaecytisus palmensis from Australia; and Pyrenochaeta oryzae in M. charantia from Thailand which after getting susceptible host and favourable environmental conditions could get established and cause severe damage to the crop either by reducing yield or by affecting the seed germination.

Xanthomonas campestris pv. campestris (Pammel) Dowson, the causal agent of black rot of crucifers was intercepted in B. carinata (2.20%) and B. rapa (2.33%) from Canada, in B. o. var. botrytis from The Netherlands (1.51%); in B. o. var. capitata from The Netherlands (20.00%); in B. juncea from Canada (0.29%). The bacterial colonies isolated from brassicas were yellow, raised, convex, shiny and mucoid on yeast glucose chalk agar medium. The bacterium was aerobic, Gram-negative, rod-shaped, 0.7 − 3.0 × 0.4 − 0.5 μm, motile with a single polar flagellum. It did not reduce nitrates but hydrolyzed starch, casein and gelatin. The bacterium produced acid from arabinose, dextrose, galactose, glycerol, maltose, mannitol, raffinose and saccharose and identified as X. c. pv. campestris (Schaad et al. 2001; Shekhawat et al. 1982). The bacterium is reported to survive in seeds up to three years (CAB International, 2007) and seed infection as low as 0.03% can cause epidemic in a field (Vicente et al. 2001). Cruz et al. (2017) reported existence of 11 races in X. c. pv. campestris. Singh et al. (2016) have also reported three races in this pathogen from India. In past, X. c. pv. campestris was intercepted in brassicas from 38 countries (Singh et al. 2006).

The methods for detection were selected based on specific pathogens and best methods of detection were used for particular pathogen like washing test was used for Pernospora manushurica and Puccinia carthami. Incubation method using blotter test was used for detection of other fungal pathogens wherever fungal growth including conidia/fruiting bodies are required to identify the pathogens. Out of 2123 infected/contaminated seeds and vegetative propagules, 1457 (68.63%) samples were salvaged by using various suitable techniques and remaining 666 (31.37%) samples were rejected and incinerated. The infected/contaminated seeds of O. sativa (56), Carthamus spp. (244) and T. aestivum (5) with U. viurens, P. carthami and T. foetida, respectively, were removed mechanically followed by ethyl alcohol wash and drying (Dev et al. 2012). Nine seed samples of Brassicas infected with X. c. pv. campestris were subjected to HWT at 50 °C for 20 min (Singh et al. 2006). Rest of the infected/contaminated seed samples of different crops were treated with a mixture of the fungicides, carbendazim @ 0.5 g + mancozeb @ 1.25 g kg−1 seed prior to release. Prophylactic HWT at 52 °C for 30 min was given to all the Oryza sativa samples. Prophylactic fungicidal dip treatment with a mixture of mancozeb @ 1.25 g + carbendazim @ 0.5 g l−1 of water followed by insecticide malathion @ 0.05% for 10 min was given to all the vegetative propagules to safeguard against associated pests.

Further, risk analysis revealed that among pathogens of quarantine potential (Table 2), T. barclayana was recorded with highest number of interception in 449 rice samples (45.95%) imported from several countries, of which 306 samples were from China alone. This clearly indicates that import of rice from China is of high risk. Similarly, Fusarium solani was recorded with second highest interception in 117 samples (3.9%) of which, 26 samples of different crops were recorded from USA alone. P. manshurica, a host specific pathogen of soybean, was intercepted in 16 samples (1.50%), of which, highest interception (10 samples) was recorded only from Canada. This revealed that there is a high risk of introduction of P. manshurica in importing soybean from Canada than other countries during this period.
Table 2

Important interceptions of pathogens of quarantine significance from various countries

Pathogen

Total infected samples (No.)

Country wise share of interception

Country

Infected samples (No.)

Interception (%)

A. pisi

12

Syria

12

100.00

B. maydis

16

Thailand

9

56.25

D. macrospora

2

Thailand

2

100.00

F. oxysporum

11

USA

4

36.36

F. o. f. sp. cucumerina

1

USA

1

100.00

F. solani

117

USA

26

22.22

P. manshurica

16

Canada

10

62.50

P. exigua f sp. exigua

14

Thailand

7

50.00

P. lingam

2

Canada

1

50.00

T. barclayana

449

China

306

68.15

V. albo-atrum

17

Netherlands

12

70.59

X. c. pv. campestris

9

Canada

5

55.56

Depending on number of samples of crops imported, highest risk of introduction of quarantine pathogen is involved in import of G. max (12.41%) followed by O. sativa (5.21%).

Country wise import revealed that highest interceptions were made from USA (673 samples), out of which 31 samples were infected with pathogens of quarantine significance (F. oxysporum, F. o. f. sp. cucumerina and F. solani) and 642 samples with other pathogens of economic importance. The second highest interception was recorded from China (306) and all were infected with non-regulated quarantine pathogen (T. barclayana). This observation revealed that declaration in the phytosanitary certificate does not guarantee the introduction of pathogen(s)-free PGR.

Therefore, while importing PGR from any country, there is a need to examine the samples very critically including sensitive diagnostic tools to prevent entry of the pathogen(s) associated with PGR. Interception of large number of pathogens of quarantine significance on a wide range of crops from different countries emphasizes the importance of constant vigil leading to safe introduction of PGR required for crop improvement programmes in the country. Such interceptions would go a long way in ensuring biosecurity by preventing the introduction of new pathogens/or more virulent races into the country.

Notes

Acknowledgements

The authors are thankful to The Director, ICAR-NBPGR, New Delhi for providing facilities. The authors also acknowledge the help of the staff of Division of Plant Quarantine in processing the samples during joint inspection for quarantine clearance.

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Copyright information

© Indian Phytopathological Society 2018

Authors and Affiliations

  • Baleshwar Singh
    • 1
  • Jameel Akhtar
    • 1
  • Aravindaram Kandan
    • 1
  • Pardeep Kumar
    • 1
  • Dinesh Chand
    • 2
  • Ashok Kumar Maurya
    • 1
  • Prakash Chand Agarwal
    • 1
  • Sunil Chandra Dubey
    • 1
  1. 1.Division of Plant QuarantineICAR-National Bureau of Plant Genetic ResourcesPusa CampusIndia
  2. 2.Regional StationICAR-National Bureau of Plant Genetic ResourcesAkolaIndia

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