Multi-Gene Phylogenetic Approach for Identification and Diversity Analysis of Bipolaris maydis and Curvularia lunata Isolates Causing Foliar Blight of Zea mays
Abstract
:1. Introduction
2. Materials and Methods
2.1. Collection of Maydis-Leaf-Blight-Symptomatic Samples from Major Maize-Growing Regions of India
Sampling
2.2. Isolation and Morphological Characterization of Pathogens
2.3. Molecular Characterization
2.3.1. DNA Extraction, PCR, and Sequencing
2.3.2. Amplification and Purification of PCR Products
2.3.3. Sequence Alignment and Phylogenetic Analyses
2.3.4. Statistical Analysis
Isolates Code | Host | Location | Identified Organism | ITS1 and ITS4 Accession Number | GAPDH Accession Number | LSU Accession Number | D1 and D2 Region of LSU Accession Number | NAIMCC Accession Number | Reference |
---|---|---|---|---|---|---|---|---|---|
E43 | Zea mays | Hariharpur, Sant Kabir Nagar, Uttar Pradesh, India | Curvularia lunata | MH104636 | LC543643 | MT416023 | LC546663 | NAIMCC-F-03913 | This study |
E36 | Zea mays | Ludhiana, Punjab, India | Curvularia lunata | MH104637 | LC543644 | MT416024 | LC546664 | Yet to be submitted | This study |
E50 | Zea mays | Pantnagar, Udham Singh Nagar, Uttarakhand, India | Bipolaris maydis | MH145411 | LC543968 | MT416015 | LC546657 | NAIMCC-F-03997 | This study |
E7 | Zea mays | Nagla, Udham Singh Nagar, Uttarakhand, India | Bipolaris maydis | MH145412 | LC508971 | MT416016 | LC546658 | NAIMCC-F-03919 | This study |
E10 | Zea mays | HardasChak, Khagaria, Bihar, India | Bipolaris maydis | MH145413 | LC543969 | MT416017 | LC546659 | NAIMCC-F-03990 | This study |
E15 | Zea mays | Godargama, Begusarai, Bihar, India | Bipolaris maydis | MH145414 | LC538220 | MT416018 | LC546660 | NAIMCC-F-03991 | This study |
E13 | Zea mays | Khargajepur, MauNath Bhanjan Uttar Pradesh, India | Curvularia lunata | MH183189 | LC524133 | MT416004 | LC546646 | NAIMCC-F-03917 | This study |
E27 | Zea mays | KhiriyaMau Nath BhanjanUttar Pradesh, India | Bipolaris maydis | MH183190 | LC544122 | MT416005 | LC546647 | NAIMCC-F-03916 | This study |
E25 | Zea mays | Kasuet, MaunathBhanjanUttar Pradesh, India | Bipolaris maydis | MH183191 | LC529408 | MT416006 | LC546648 | NAIMCC-F-03988 | This study |
E37 | Zea mays | Ludhiana, Punjab, India | Curvularia lunata | MH183192 | LC544123 | MT416007 | LC546649 | NAIMCC-F-03915 | This study |
E41 | Zea mays | Azamgarh, Uttar Pradesh, India | Curvularia lunata | MH183193 | LC529749 | MT416008 | LC546650 | NAIMCC-F-03914 | This study |
E16 | Zea mays | Sari Tole SanicharaAsthan, Samastipur, Bihar, India | Curvularia lunata | MH183194 | LC538355 | MT416009 | LC546651 | Yet to be submitted | This study |
E39 | Zea mays | Mau Nath BhanjanUttar Pradesh, India | Curvularia lunata | MH183195 | LC544124 | MT416010 | LC546652 | Yet to be submitted | This study |
E12 | Zea mays | Singhaw, FatehpurUttarPradesh, India | Curvularia lunata | MH183196 | LC508972 | MT416011 | LC546653 | NAIMCC-F-03918 | This study |
E19 | Zea mays | Saidpur Ama, Begusarai, Bihar | Bipolaris maydis | MH183197 | LC541581 | MT416012 | LC546654 | NAIMCC-F-03992 | This study |
E34 | Zea mays | Ludhiana, Punjab, India | Curvularia lunata | MH183198 | LC545392 | MT416013 | LC546655 | Yet to be submitted | This study |
E3 | Zea mays | Godargama, Begusarai, Bihar, India | Bipolaris maydis | MT799977 | LC538353 | MT799989 | LC546665 | NAIMCC-F-03989 | This study |
E14 | Zea mays | Lakho, Begusarai, Bihar, India | Curvularia lunata | MT799978 | LC538354 | MT799990 | LC546666 | NAIMCC-F-04001 | This study |
E24 | Zea mays | Jigni, Rohtas, Bihar, India | Bipolaris maydis | MT524321 | LC552295 | MT516300 | MT533838 | NAIMCC-F-03993 | This study |
E30 | Zea mays | BhindKund, Ballia, Uttar Pradesh, India | Bipolaris maydis | MT524322 | LC552288 | MT516301 | MT533839 | NAIMCC-F-03998 | This study |
E35 | Zea mays | Ludhiana, Punjab, India | Curvularia lunata | MT524323 | LC552292 | MT516302 | MT533840 | Yet to be submitted | This study |
E28 | Zea mays | Bhar, MauNathBhanjan, Uttar Pradesh, India | Curvularia lunata | MT524324 | LC552287 | MT516303 | MT533841 | Yet to be submitted | This study |
E33 | Zea mays | Khojpur, Jalandhar, Punjab, India | Curvularia lunata | MT524325 | LC552290 | MT516304 | MT533842 | NAIMCC-F-03986 | This study |
E6 | Zea mays | Talwandi Bharo, Jalandhar, Punjab, India | Curvularia lunata | MT524326 | LC552294 | MT516305 | MT533843 | Yet to be submitted | This study |
E38 | Zea mays | Jalandhar, Punjab, India | Bipolaris maydis | MT524327 | LC552293 | MT516306 | MT533844 | NAIMCC-F-03996 | This study |
E32 | Zea mays | Allowal, Punjab, India | Curvularia lunata | MT524328 | LC552289 | MT516307 | MT533845 | Yet to be submitted | This study |
E31 | Zea mays | BarharaChargaha, Maharajganj, Uttar Pradesh, India | Curvularia lunata | MT524329 | LC552683 | MT516308 | MT533846 | NAIMCC-F-04002 | This study |
E26 | Zea mays | Mustafabad, FaizabadUttar Pradesh, India | Bipolaris maydis | MT524331 | LC552286 | MT516310 | MT533848 | NAIMCC-F-03994 | This study |
AR 5183 | Zea mays | Japan | Bipolaris maydis | KM230390 | KM034848 | NA | NA | NA | [11] |
CBS 136.29 | Zea mays | Japan | Bipolaris maydis | KJ909769 | KM034845 | NA | NA | NA | [11] |
AR 5182 | Zea mays | Japan | Bipolaris maydis | KM230388 | KM034844 | NA | NA | NA | [11] |
CBS 137271/C5 | Zea mays | USA | Bipolaris maydis | AF071325 | KM034846 | NA | NA | NA | [11] |
CBS137271/C5 | Zea mays | USA | Bipolaris maydis | AF071325 | KM034846 | KM243280 | NA | NA | [11] |
Zea mays | NA | ||||||||
CBS157.34 | Indonesia | Bipolaris maydis | JX256430 | JX276442 | - | NA | NA | [42] | |
CPC 28832 | Triticum aestivum | Thailand | Bipolaris sorokiniana | MF490812 | MF490834 | - | NA | NA | [59] |
M 1122/C4 | Zea mays | USA | Bipolaris maydis | KM230389 | KM034847 | - | NA | NA | [11] |
CBS 108941 | NA | = | Dreschlera erythrospila | AY004782 | AY004813 | - | NA | NA | [60] |
MFLUCC 10-0706 | Oryza sativa, | Thailand | Curvularia lunata | JX256431 | JX276443 | JX256398 | NA | NA | [11] |
CBS730.96 | Human lung biopsy | USA | Curvularia lunata | JX256429 | JX276441 | JX256396 | NA | NA | [11] |
MFLUCC 10-0695 | Panicum sp. | Thailand | Curvularia lunata | JX256432 | JX276444 | JX256399 | NA | NA | [11] |
CBS 136.29 | Zea mays | Japan | Bipolaris maydis | KJ909769 | KM034845 | - | NA | NA | [11] |
CBS 307.64 | Zea mays | USA | Bipolaris maydis | HF934925 | HG779085 | HF934875 | NA | NA | [61] |
CBS 130.26 | Zea mays | - | Bipolaris maydis | HF934923 | HG779084 | HF934873 | NA | NA | [61] |
CBS573.73 | Zea mays | USA | Bipolaris maydis | HF934924 | NA | MH872501 | HF934881 | NA | [61] |
CBS 307.84 | Avena sativa | Sweden | Pyrenophora avenicola | MK539972 | MK540180 | MK540042 | NA | NA | [62] |
CBS330.53 | = | Japan | Rhizopus oryzae | MH857229 | NA | MH868766 | NA | NA | [63] |
ICMP 6128 | Cynodon dactylon | New Zealand | Bipolaris cynodontis | JX256412 | JX276427 | JX256380 | NA | NA | [42] |
BRIP 12898 | Melinis munitiflora | Australia | Bipolaris melinidis | JN601035 | JN600972 | JX256411 | NA | NA | [42] |
CBS 280.91 | Microlaenae stipoidis | Australia | Bipolaris microlaenae | JN601032 | JN600974 | JN600995 | NA | NA | [42] |
MFLUCC 10-0694 | Oryza sativa | Thailand | Bipolaris oryzae | JX256413 | JX276428 | JX256381 | NA | NA | [42] |
BRIP 12790 | Cynodon dactylon | Australia | Bipolaris peregianensis | JN601034 | JN600977 | JN601000 | NA | NA | [42] |
MFLUCC 10-0705 | Panicum sp. | Thailand | Curvularia alcornii | JX256421 | JX276434 | JX256388 | NA | NA | [42] |
MFLUCC 10-0687 | Oryza sativa | Thailand | Curvularia asianensis | JX256422 | JX276435 | JX256389 | NA | NA | [42] |
CBS 193.62 | Air | Pakistan | Curvularia ellisii | JN192375 | JN600963 | JN600985 | NA | NA | [42] |
ICMP 6160 | Gladiolus sp. | New Zealand | Curvularia gladioli | JX256426 | JX276438 | JX256393 | NA | NA | [42] |
BRIP 23186a | - | Australia | Curvularia graminicola | JN192376 | JN600964 | JN600986 | NA | NA | [42] |
BRIP 15933 | Chloris gayana | Australia | Curvularia hawaiiensis | JN601028 | JN600965 | JN600987 | NA | NA | [42] |
CBS 284.91 | Heteropogon contortus | Australia | Curvularia heteropogonis | JN192379 | JN600969 | JN600990 | NA | NA | [42] |
ICMP 6172 | Ischaemum indicum | Solomon Islands | Curvularia ischaemi | JX256428 | JX276440 | JX256395 | NA | NA | [42] |
BRIP 15882a | Eragrostis interrupta | Australia | Curvularia ovariicola | JN601031 | JN600971 | JN600992 | NA | NA | [42] |
BRIP 13165a | Sporobolus fertilis | Australia | Curvularia ravenelii | JN192386 | JN600978 | JN601001 | NA | NA | [42] |
CBS 274.52a | Soil | Spain | Curvularia spicifera | JN192387 | JN600979 | JX256400 | NA | NA | [42] |
BRIP 12375 | Unknown | Australia | Curvularia tripogonis | JN192388 | JN600980 | JN601002 | NA | NA | [42] |
CBS 146.63 | Unknown | India | Curvularia tuberculata | MH858243 | LT715830 | MH869845 | NA | NA | [42] |
CBS 192.29 | Japan | Curvularia coicis | MH855040 | HG779130 | MH866505 | NA | NA | [63] | |
BRIP 14845 | Coffea arabica | Kenya | B. coffeana | KJ415525 | KJ415421 | KJ415478 | NA | NA | [64] |
BRIP 12530 | Dactyloctenium radulan | Australia | B. clavate | KJ415524 | KJ415422 | KJ415477 | NA | NA | [64] |
CBS274.91 | Eleusine indica | USA | Bipolaris eleusines | KJ909768 | KM034820 | KM243289 | NA | NA | [11] |
BRIP 14838 | Croton sp. | - | Bipolaris crotonis | KJ415526 | KJ415420 | KJ415479 | NA | NA | [64] |
CBS 109894 | C. dactylon | Hungary | Bipolaris cynodontis | KJ909767 | KM034838 | KM243288 | NA | NA | [11] |
CBS241.92 | Hevea sp. | Nigeria | B.heveae | KJ909763 | KM034843 | KM243294 | NA | NA | [11] |
BRIP 14840 | Gossypium sp. | Kenya | B. gossypina | KJ415528 | KJ415418 | KJ415481 | NA | NA | [11] |
BRIP 15613 | Microlaena stipoides | Australia | B. microlaenae | JN601032 | JN600974 | JN600995 | NA | NA | [18] |
CBS 199.29 | P. miliaceum | Japan | B. panici-miliace | KJ909773 | KM042896 | KM243281 | NA | NA | [18] |
BRIP 12790 | C. dactylon | Australia | B. peregianensis | JN601034 | JN600977 | JN601000 | NA | NA | [18] |
BRIP 14839 | E. coracana | Zambia | B. pluriseptata | KJ41553 | KJ415414 | KJ41548 | NA | NA | [64] |
IMI 228224 | Salvinia auriculata | Brazil | B. salviniae | KJ922390 | KM034829 | KM243283 | NA | NA | [11] |
CBS 120.24 | Italy | B. sorokiniana | KJ909776 | KM034821 | KM243278 | NA | NA | [11] | |
CBS 624.68 | Dichanthium annulatum | USA | C. robusta | KJ909783 | KM083613 | KM243297 | NA | NA | [11] |
CBS 349.90 | S. creber | Australia | C. riley | KJ909766 | KM083612 | KM243267 | NA | NA | [11] |
CBS 239.48 | - | USA | Curvularia portulacae | MH856324 | LT715903 | MH867878 | NA | NA | [63] |
CBS 350.90a | Perotis rara | Australia | Curvularia perotidis | JN192385 | HG779138 | JN600999 | NA | NA | [18] |
CBS 156.35 | Air | Jawa | C. pallescens | KJ922380 | KM083606 | KM243269 | NA | NA | [11] |
CBS 160.58 | Eleusine Indica | USA | C. nodulosa | JN601033 | JN600975 | JN600997 | NA | NA | [11] |
CBS 656.74 | Desert soil | Egypt | C. subpapendorfii | KJ909777 | KM061791 | KM243266 | NA | NA | [11] |
CBS 327.64 | Avena sativa | USA | B. victoriae | KJ909778 | KM034811 | KM243271 | NA | NA | [11] |
BRIP 17186 | Heliconia psittacorum | Australia | Bipolaris heliconiae | KJ415530 | KJ415417 | KJ415483 | NA | NA | [64] |
BRIP 15900 | Sorghum bicolor | Australia | Curvularia sorghina | KJ415558 | KJ415388 | KJ415512 | NA | NA | [64] |
BRIP 14845 | Coffea arabica | Kenya | Bipolaris coffeana | KJ415525 | KJ415421 | KJ415478 | NA | NA | [64] |
E29 | Zea mays | India | Curvularia geniculata | MT524330 | LC552684 | MT533847 | NA | NA | [49] |
3. Results
3.1. Morphological Identification of Bipolaris Isolates (Maydis Leaf Blight)
3.2. Morphological Identification of Curvularia Isolates (Maize Leaf Spot)
3.3. Pathogenicity of the Isolate
3.4. Phylogenetic Study of Bipolaris Isolates (Causal Organism of Maydis Leaf Blight)
3.4.1. Phylogeny Based on the Ribosomal Marker ITS Regions of Bipolaris maydis
3.4.2. Phylogenetic Analysis of ITS + GAPDH Gene of Bipolaris maydis
3.4.3. Phylogeny Based on the ITS + LSU Gene of Bipolaris maydis
3.4.4. Phylogeny Based on the ITS + LSU + GAPDH Gene of Bipolaris maydis
3.5. Phylogenetic Study of Curvularia lunata Isolates (Causal Organism of Maize Leaf Spot)
3.5.1. Phylogeny Based on the ITS of Curvularia lunata
3.5.2. Phylogeny Based on the ITS + GAPDH of Curvularia lunata
3.5.3. Phylogeny Based on the ITS + LSU of Curvularia lunata
3.5.4. Phylogeny Based on the Multigene of Curvularia lunata
3.6. Phylogenetic Studies between Bipolaris and Curvularia Complex
3.6.1. Phylogeny Based on the Combined Sequences of ITS + GAPDH of Bipolaris maydis and Curvularia lunata
3.6.2. Phylogeny Based on the Combined Sequences of ITS + LSU of Bipolaris maydis and Curvularia lunata
3.6.3. Phylogeny Based on the Combined Regions Multigene for Bipolaris and Curvularia Complex
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
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S. No. | Sampling Sites | District Coordinates (Latitude and Longitude) | Maydis-Leaf-Blight-Symptomatic Samples (186) | Maize Leaf Spot Samples (129) |
---|---|---|---|---|
1. | Jaunpur, Uttar Pradesh | 25.62 N; 82.98 E | 09 | 07 |
2. | Sant Kabir Nagar, Uttar Pradesh | 25.59 N; 82.98 E | 06 | 04 |
3. | Faizabad, Uttar Pradesh | 26.73 N; 82.15 E | 04 | 03 |
4. | Maharajganj, Uttar Pradesh | 27.22 N; 83.82 E | 09 | 05 |
5. | MauNathBhanjan, Uttar Pradesh | 25.87 N; 83.47 E | 15 | 04 |
6. | Ballia, Uttar Pradesh | 25.77 N; 84.16 E | 13 | 07 |
7. | Azamgarh, Uttar Pradesh | 25.73 N; 82.99 E | 09 | 05 |
8. | Udham Singh Nagar, Uttarakhand | 28.99 N; 79.51 E | 13 | 05 |
9. | Almora, Uttarakhand | 29.62 N; 79.67 E | 07 | 08 |
10. | Haldwani, Uttarakhand | 29.16 N; 79.51 E | 06 | 03 |
11. | Samastipur, Bihar | 25.87 N; 85.81 E | 08 | 11 |
12. | Khagaria, Bihar | 25.51 N; 86.50 E | 12 | 07 |
13. | Begusarai, Bihar | 25.38 N; 86.18 E | 18 | 12 |
14. | Rohtas, Bihar | 24.63 N; 83.92 E | 06 | 06 |
15. | Baruni, Bihar | 25.45 N; 86.00 E | 09 | 07 |
16. | Bhagalpur, Bihar | 25.25 N; 86.95 E | 06 | 04 |
17. | Katihar, Bihar | 25.39 N; 87.63 E | 08 | 02 |
18. | Ludhiana, Punjab | 30.90 N; 75.79 E | 09 | 11 |
19. | Jalandhar, Punjab | 30.99 N; 75.74 E | 11 | 06 |
20. | Allowal, Punjab | 31.15 N; 75.67 E | 08 | 12 |
Group | Colony Characteristics | Conidia | ||
---|---|---|---|---|
Average Length (µm) | Average Width (µm) | Shape | ||
A (n = 20) | Grey with white spots, rough raised mycelia, irregular margin | 80.44 ± 0.71 a (64–89) | 14.64 ± 0.28 ab (13–16) | Fusiform, slightly curved, dark brown, 4–9 distoseptate |
B (n = 9) | Grey, smooth raised mycelia, irregular margin | 65.38 ± 0.64 e (53–71) | 12.43 ± 0.59 d (11–13) | Fusiform, slightly curved, light brown, 4 distoseptate |
C (n = 25) | Grey, smooth appressed mycelia, irregular margin | 74.05 ± 0.14 c (63–97) | 15.14 ± 0.35 a (14–16) | Brown, 6–8 distoseptate |
D (n = 11) | Blackish grey with white spot, smooth appressed mycelia, regular margin | 76.68 ± 0.54 b (68–84) | 13.44 ± 0.44 c (12–14) | Brown, 4–5 distoseptate |
E (n = 12) | Whitish grey, rough raised mycelia, irregular margin | 71.29 ± 0.80 d (51–83) | 13.89 ± 0.38 bc (12–15) | Light brown, 5–9 distoseptate |
Group | Colony Characteristics | Conidia | ||
---|---|---|---|---|
Average Length | Average Width | Shape | ||
F (n = 15) | Black, smooth velvety mycelia, regular margin | 20.86 ± 0.85 bc (19–22) | 10.23 ± 0.35 b (8–11) | Light brown, 3–4 distoseptate |
G (n = 8) | Grey, smooth floccose mycelia, irregular margin | 27.29 ± 0.79 a (25–29) | 12.71 ± 0.72 a (12–13) | Light yellow, 3–4 distoseptate |
H (n = 21) | Grey, smooth appressed mycelia, irregular margin | 29.15 ± 0.27 a (25–35) | 11.96 ± 0.78 a (10–12) | Brown, 4–5 distoseptate |
I (n = 14) | Blackish grey, smooth appressed mycelia, regular margin | 19.69 ± 0.46 c (16–24) | 9.58 ± 0.44 b (9–10) | Light brown, 3–4 distoseptate |
J (n = 16) | Whitish grey, smooth velvety mycelia, regular margin | 22.82 ± 0.24 b (22–23) | 8.77 ± 0.67 b (8–9) | Light brown, 3–4 distoseptate |
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Manzar, N.; Kashyap, A.S.; Maurya, A.; Rajawat, M.V.S.; Sharma, P.K.; Srivastava, A.K.; Roy, M.; Saxena, A.K.; Singh, H.V. Multi-Gene Phylogenetic Approach for Identification and Diversity Analysis of Bipolaris maydis and Curvularia lunata Isolates Causing Foliar Blight of Zea mays. J. Fungi 2022, 8, 802. https://doi.org/10.3390/jof8080802
Manzar N, Kashyap AS, Maurya A, Rajawat MVS, Sharma PK, Srivastava AK, Roy M, Saxena AK, Singh HV. Multi-Gene Phylogenetic Approach for Identification and Diversity Analysis of Bipolaris maydis and Curvularia lunata Isolates Causing Foliar Blight of Zea mays. Journal of Fungi. 2022; 8(8):802. https://doi.org/10.3390/jof8080802
Chicago/Turabian StyleManzar, Nazia, Abhijeet Shankar Kashyap, Avantika Maurya, Mahendra Vikram Singh Rajawat, Pawan Kumar Sharma, Alok Kumar Srivastava, Manish Roy, Anil Kumar Saxena, and Harsh Vardhan Singh. 2022. "Multi-Gene Phylogenetic Approach for Identification and Diversity Analysis of Bipolaris maydis and Curvularia lunata Isolates Causing Foliar Blight of Zea mays" Journal of Fungi 8, no. 8: 802. https://doi.org/10.3390/jof8080802