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Characterizing the Interaction Between Root-knot Nematodes and Soil-borne Fungi which are Pathogenic to Passion Fruit (Passiflora edulis)

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Figure 1

Effect of Meloidogyne incognita and Neocosmospora sp. 311, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.
Effect of Meloidogyne incognita and Neocosmospora sp. 311, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.

Figure 2

Effect of Meloidogyne javanica and Neocosmospora sp. 311, acting alone orcombined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.
Effect of Meloidogyne javanica and Neocosmospora sp. 311, acting alone orcombined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.

Figure 3

Effect of Meloidogyne incognita and Neocosmospora sp. 511, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.
Effect of Meloidogyne incognita and Neocosmospora sp. 511, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.

Figure 4

Effect of Meloidogyne javanica and Neocosmospora sp. 511, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.
Effect of Meloidogyne javanica and Neocosmospora sp. 511, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.

Figure 5

Effect of Meloidogyne incognita and Fusarium nirenbergiae 022, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.
Effect of Meloidogyne incognita and Fusarium nirenbergiae 022, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.

Figure 6

Effect of Meloidogyne javanica and Fusarium nirenbergiae 022, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.
Effect of Meloidogyne javanica and Fusarium nirenbergiae 022, acting alone or combined, on the growth of passion fruit plants cultivated in a growth chamber, in the assays 1 (dotted column) and 2 (brick-pattern column). F: parasitism by fungus only; N: parasitism by nematode only; F + N: parasitism by fungus and nematode; C: noninoculated control. Columns with different letters indicate significant difference between treatments according to the Tukey test at 5%. Values are mean of 10 replicates per treatment for each assay.

Figure S1

(A) Aspect of passion fruit plants in growth chamber assay to investigate fungusnematode interactions; (B) width of collar lesion caused by Fusarium nirenbergiae F022; (C) length of collar lesions caused by F. nirenbergiae F022 (two stems on the left) and Neocosmospora sp.; (D) fungus re-isolation from lesioned tissues.
(A) Aspect of passion fruit plants in growth chamber assay to investigate fungusnematode interactions; (B) width of collar lesion caused by Fusarium nirenbergiae F022; (C) length of collar lesions caused by F. nirenbergiae F022 (two stems on the left) and Neocosmospora sp.; (D) fungus re-isolation from lesioned tissues.

Figure S2

Range of symptoms observed in passion fruit plants in growth chamber assays to investigate the interactions Meloidogyne incognita-Neocosmospora sp. 311 (top row); M. incognita-Neocosmospora sp. 511 (middle row); and M. incognita-Fusarium nirenbergiae F022 (bottom row). (A) non-inoculated control; (B) parasitized by nematode only; (C) parasitized by fungus only; (D) co-parasitized by nematode and fungus.
Range of symptoms observed in passion fruit plants in growth chamber assays to investigate the interactions Meloidogyne incognita-Neocosmospora sp. 311 (top row); M. incognita-Neocosmospora sp. 511 (middle row); and M. incognita-Fusarium nirenbergiae F022 (bottom row). (A) non-inoculated control; (B) parasitized by nematode only; (C) parasitized by fungus only; (D) co-parasitized by nematode and fungus.

Figure S3

Range of symptoms observed in passion fruit plants in growth chamber assays to investigate the interactions Meloidogyne javanica-Neocosmospora sp. 311 (top row); M. javanica-Neocosmospora sp. 511 (middle row); and M. javanica-Fusarium nirenbergiae F022 (bottom row). (A) non-inoculated control; (B) parasitized by nematode only; (C) parasitized by fungus only; (D) co-parasitized by nematode and fungus.
Range of symptoms observed in passion fruit plants in growth chamber assays to investigate the interactions Meloidogyne javanica-Neocosmospora sp. 311 (top row); M. javanica-Neocosmospora sp. 511 (middle row); and M. javanica-Fusarium nirenbergiae F022 (bottom row). (A) non-inoculated control; (B) parasitized by nematode only; (C) parasitized by fungus only; (D) co-parasitized by nematode and fungus.

. P values obtained in the Shapiro–Wilk test at 5% for the effect of pathogens, acting alone or combined, on passion fruit plants cultivated in replicated growth chamber assays (1 and 2).

Assays Variables and interactions
SM RSM PL SL RSV
Meloidogyne incognita -Neocosmopora sp. 311
1 0.21 0.34 0.08 0.07 6.53 × 10–9
2 0.37 0.17 0.63 0.52 0.005
M. incognita Neocosmopora sp. 511
1 0.41 0.31 0.07 0.1 5.61 × 10–6
2 0.69 0.26 0.74 0.07 3.74 × 10–12
M. incognita Fusarium nirenbergiae F022
1 0.27 0.46 0.2 0.71 7.74 × 10–6
2 0.76 0.52 0.81 0.24 5.21 × 10–6
Meloidogyne javanica -Neocosmopora sp. 311
1 0.98 0.11 0.33 0.55 0.0001
2 0.99 0.17 0.79 0.33 1.84 × 10–12
M. javanica- Neocosmopora sp. 511
1 0.08 0.51 0.31 0.4 0.02
2 0.14 0.92 0.57 0.64 4.26 × 10–8
M. javanica -F. nirenbergiae F022
1 0.09 0.86 0.06 0.39 0.046
2 0.63 0.4 0.63 0.38 1.84 × 10–12

Severity of shoot symptoms, ranked on a 1–5 scale, induced by pathogens acting alone or combined in passion fruits plants cultivated in replicated growth chamber assays (1 and 2).

Treatments Interactions and assays
Meloidogyne incognita-Neocosmospora sp. 311
1 2
Neocosmospora sp. 311 3.1 ba 3.5 b
M. incognita 0.9 a 1.4 a
M. incognita-Neocosmospora sp. 311 3.3 b 3.4 b
Uninoculated control 1 a 1 a
M. incognita-Neocosmospora sp. 511
1 2
Neocosmospora sp. 511 2 b 3.2 bc
M. incognita 2.3 b 3 b
M. incognita-Neocosmospora sp. 511 2 b 3.8 c
Uninoculated control 1 a 1 a
M. incognita-Fusarium nirenbergiae F022
1 2
F. nirenbergiae F022 3.6 c 3 b
M. incognita 2.3 b 3 b
M. incognita-F. nirenbergiae F022 2.7 bc 3 b
Uninoculated control 1 a 1 a
Meloidogyne javanica-Neocosmospora sp. 311
1 2
Neocosmospora sp. 311 3.7 c 3 b
M. javanica 2.6 b 3 b
M. javanica-Neocosmospora sp. 311 3.3 bc 3.2 b
Uninoculated control 1 a 1 a
Meloidogyne javanica-Neocosmospora sp. 511
1 2
Neocosmospora sp. 511 2.4 b 3 b
M. javanica 2 b 3 b
M. javanica-Neocosmospora sp. 511 2.1 b 3.2 b
Uninoculated control 1 a 1 a
M. javanica-F. nirenbergiae F022
1 2
F. nirenbergiae F022 3.1 b 3 b
M. javanica 3 b 3 b
M. javanica-F. nirenbergiae F022 3 b 3.3 b
Uninoculated control 2 a 1 a

Effect of pathogens, acting alone or combined, on the root system volume (in mm3) of passion fruits plants cultivated in replicated growth chamber assays (1 and 2).

Treatments Interactions and assays
Meloidogyne incognita-Neocosmospora sp. 311
1 2
Neocosmospora sp. 311 1500 aa 1400 b
M. incognita 1000 a 1700 b
M. incognita-Neocosmospora sp. 311 1000 a 1400 b
Uninoculated control 1000 a 2900 a
M. incognita-Neocosmospora sp. 511
1 2
Neocosmospora sp. 511 1800 a 1100 a
M. incognita 1000 b 1100 a
M. incognita-Neocosmospora sp. 511 1000 b 1100 a
Uninoculated control 1200 b 1100 a
M. incognita-Fusarium nirenbergiae F022
1 2
F. nirenbergiae F022 1000 a 1000 a
M. incognita 1400 a 1400 a
M. incognita-F. nirenbergiae F022 1000 a 1000 a
Uninoculated control 1300 a 1200 a
Meloidogyne javanica-Neocosmospora sp. 311
1 2
Neocosmospora sp. 311 1500b c 1000 a
M. javanica 2400 ab 1000 a
M. javanica-Neocosmospora sp. 311 1400 bc 1000 a
Uninoculated control 2400 a 1000 a
M. javanica-Neocosmospora sp. 511
1 2
Neocosmospora sp. 511 1800 a 1100 a
M. javanica 2000 a 1300 a
M. javanica-Neocosmospora sp. 511 1000 b 1000 a
Uninoculated control 2400 a 1300 a
M. javanica-F. nirenbergiae F022
1 2
F. nirenbergiae F022 2300 a 1000 a
M. javanica 2400 a 1000 a
M. javanica-F. nirenbergiae F022 2100 a 1000 a
Uninoculated control 2600 a 1000 a

Mean squares obtained in ANOVA for the effect of pathogens, acting alone or combined, on passion fruit plants cultivated in replicated growth chamber assays.

Parameters Variables and interactions
SM RSM PL SL
Meloidogyne incognita- Neocosmospora sp. 311
Assay 1.53* 0.25 288.9** 1.31
Treatment 5.9** 0.39** 209.98** 62.61**
Assay × treatment 1.03** 0.96** 19.49 18.22
Residual 0.25 0.09 19.88 9.78
CV% 44.7 54.6 12.13 17.19
M. incognita-Neocosmospora sp. 511
Assay 0.002 0.02 33.61 0**
Treatment 2.5** 0.11* 68.53** 30.78**
Assay × treatment 3.6** 0.17** 47.59* 32.26**
Residual 0.14 0.04 12.36 6.22
CV% 28.89 42.23 9.41 12.9
M. incognita-Fusarium nirenbergiae F022
Assay 0.16 0.24** 224.79** 24.16
Treatment 0.74* 0.18** 85.4* 19.32
Assay × treatment 0.86* 0.09** 54.07 24.68
Residual 0.24 0.01 24.83 10.19
CV% 39.45 35.12 12.91 16.62
Meloidogyne javanica- Neocosmospora sp. 311
Assay 1.61* 3.27** 913.95** 62.36*
Treatment 5.27** 0.5* 100.27* 20.24
Assay × treatment 2.86** 0.19 122.88** 5.83
Residual 0.35 0.18 29.01 10.72
CV% 39.13 54.9 13.11 15.29
M. javanica-Neocosmospora sp. 511
Assay 0.22 2.21** 377.41** 5.84
Treatment 1.32** 0.74** 72.12* 33.86**
Assay × treatment 0.11 0.28** 66.3* 27.16**
Residual 0.22 0.04 19.35 4.53
CV% 28.39 32.09 10.80 9.93
M. javanica-F. nirenbergiae F022
Assay 1.8** 0.48** 1207.61** 13.28
Treatment 0.98* 0.08 16.35 12.57
Assay × treatment 1.07** 0.08 85.72* 21.38
Residual 0.26 0.05 27.59 9.59
CV% 30.45 41.85 12.82 15.79

Effect of the parasitism by Meloidogyne incognita or M. javanica on the volume of lesioned tissue in the collar-stem region (in mm3) caused by Neocosmospora sp. (311 or 511) or Fusarium nirenbergiae F022 in passion fruit plants cultivated in replicated growth chamber assays (1 and 2).

Treatments Assays
1 2
Neocosmospora sp. 311 62.78 aa 41.99 a
M. incognita-Neocosmospora sp. 311 101.94 a 30.23 a
1 2
Neocosmospora sp. 511 82.64 a 36.04 a
M. incognita-Neocosmospora sp. 511 72.24 a 38.03 a
1 2
F. nirenbergiae F022 167.58 a 20.77 a
M. incognita-F. nirenbergiae F022 84.64 a 28.56 a
1 2
Neocosmospora sp. 311 162.42 a 47.79 a
M. javanica-Neocosmospora sp. 311 95.55 a 33.13 a
1 2
Neocosmospora sp. 511 111.24 a 49.21 a
M. javanica-Neocosmospora sp. 511 90.22 a 40.82 a
1 2
F. nirenbergiae F022 127.06 a 18.26 a
M. javanica-F. nirenbergiae F022 125.41 a 29.76 a

Effect of the parasitism by Neocosmospora sp. (311 or 511) or Fusarium nirenbergiae F022 on the Pf and RF of Meloidogyne incognita and M. javanica in passion fruit plants cultivated in replicated growth chamber assays (1 and 2).

Treatments Variables and assays
Pf RF
1 2 1 2
M. incognita 1570 aa 677 b 0.44 a 0.19 b
M. incognita-Neocosmospora 311 1180 b 1835 a 0.33 b 0.52 a
1 2 1 2
M. incognita 549 a 1070 a 0.15 a 0.3 a
M. incognita-Neocosmospora 511 260 b 1178 a 0.07 b 0.33 a
1 2 1 2
M. incognita 210 b 1040 a 0.06 b 0.29 a
M. incognita-F. nirenbergiae F022 414 a 780 a 0.11 a 0.22 a
1 2 1 2
M. javanica 1387 a 1820 a 0.39 a 0.52 a
M. javanica-Neocosmospora 311 445 b 1560 a 0.12 b 0.44a
1 2 1 2
M. javanica 465 b 2140 a 0.13 b 0.61 a
M. javanica-Neocosmospora 511 602 a 2260 a 0.17 a 0.64 a
1 2 1 2
M. javanica 230 a 1410 a 0.06 a 0.41 a
M. javanica-F. nirenbergiae F022 155 b 1120 a 0.04 b 0.32 a

. P values obtained in the Shapiro–Wilk test at 5% for the VLT in the collar-stem region and LL caused by Neocosmospora sp. (311 or 511) or Fusarium nirenbergiae F022, and for the Pf and RF of Meloidogyne incognita and M. javanica, in passion fruit plants cultivated in replicated growth chamber assays (1 and 2).

Assays Variables and interactions
VLT LL Pf RF
M. incognita-Neocosmopora sp. 311
1 0.12 0.28 0.08 0.08
2 0.07 0.16 1.74 × 10–5 1.74 × 10–5
M. incognita-Neocosmopora sp. 511
1 0.24 0.42 0.02 0.02
2 0.79 0.09 0.71 0.71
M. incognita-F. nirenbergiae F022
1 0.48 0.58 0.03 0.03
2 0.38 0.89 0.06 0.06
M. javanica-Neocosmopora sp. 311
1 0.36 0.59 0.002 0.002
2 0.13 0.35 0.45 0.45
M. javanica-Neocosmopora sp. 511
1 0.15 0.14 0.02 0.02
2 0.37 0.18 0.81 0.81
M. javanica-F. nirenbergiae F022
1 0.95 0.00063 0.004 0.004
2 0.12 0.0047 0.15 0.15
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