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

Mariana Z. Mangeiro; Rafael A. Nunes; José O.L. Vieira; Vicente Mussi-Dias; Alexandre P. Viana; Ricardo M. Souza

doi:10.2478/jofnem-2022-0023

Figures & Tables

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 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 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 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 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 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.

(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.

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 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 b^a	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 a^a	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 a^a	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 a^a	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

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

Figures & Tables

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Figure S1

Figure S2

Figure S3

_ 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)_

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)_

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)_

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

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)_

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)_

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