Festulolium and fungal endophyte associations: host status for Meloidogyne incognita and nematotoxic plant extracts

Festulolium genotype and endophyte number	Epichloë uncinata strain^a
FHCF0802	U2 E− (Endophyte-free)
FHCF0802 2348M	U2 E+
FHAC0802	U5 E− (Endophyte-free)
FHAC0802 ABA 10-23	U5 E+
FHCD0802	U6 E− (Endophyte-free)
FHCD0802 BUS 10-12	U6 E+
FHAB0802	U8 E− (Endophyte-free)
FHAB0802 ABA 10-22	U8 E+
FHCD0802	U10 E− (Endophyte-free)
FHCD0802 BUS 10-13	U10 E+

1 Note: aIn the text of this paper, the Festulolium/endophyte associations are generally referred to by the E. uncinata strain. For example, FHCF0802 as U2 E−, and FHCF0802 2348M as U2 E+.

Table 2.

Loline alkaloid concentrations µg/g cubic decimeter (DM) in shoots and roots of five Festulolium lines colonized by Epichloë uncinata (E+).

	Shoots					Roots
Festulolium line, endophyte, RKN^a status	NFL^b	NAL	NANL	NML	Total	NFL	NAL	NANL	NML	Total
FHCF0802, U2 E+
−RKN	5,300	1,635	1,040	428	8,403	358	0	0	0	358
+RKN	577	248	150	56	1,032	214	61	38	9	323
FHAC0802, U5 E+
−RKN	5,300	1,641	1,506	513	8,960	270	0	0	0	270
+RKN	1,294	418	541	210	2,462	415	129	89	54	687
FHCD0802, U6 E+
−RKN	4,595	949	787	679	9,121	596	0	0	0	596
FHAB0802, U8 E+
−RKN	3,419	931	689	379	5,417	551	25	14	0	590
FHCD0802, U10 E+
−RKN	3,551	853	652	397	5,453	531	17	0	0	548

1 Notes: Festulolium lines with the U2 and U5 endophyte strains were also tested after inoculation with the root-knot nematode (RKN) Meloidogyne incognita. a−RKN = not inoculated with M. incognita; +RKN = inoculated with M. incognita; bNFL = N-formylloline; NAL = N-acetylloline; NANL = N-acetylnorloline; NML = N-methylloline. Total loline = NFL + NAL + NANL + NML.

Table 3.

Meloidogyne incognita egg hatch and second-stage juvenile (J2) activity in methanolic extracts from roots and shoots of Festulolium lines FHCD0802 BUS 10-12 U6 E+ and FHCD0802 U6 E−.

	Day 5	Day 7
	% active	% active
% DMSO in controls or µg/ml extract	Shoots^a	Roots	Shoots
Water	97.1 a	94.3 a	94.3 a
Water + K^b	94.4 abc	94.5 a	94.5 a
0.5% DMSO	95.5 ab	93.7 ab	93.7 a
1.0% DMSO	94.7 ab	95.5 a	95.5 a
U6 E+ 200 µg/ml	87.8 cd	84.9 bc	85.3 b
	(8.1%)^c	–	(9.0%)
U6 E− 200 µg/ml	89.7 d	81.8 c	83.6 b
	(6.1%)	(12.7%)	(10.8%)
U6 E+ 400 µg/ml	90.8 bcd	83.3 c	79.1 b
	–	(12.8%)	(17.2%)
U6 E− 400 µg/ml	88.8 cd	78.0 c	83.6 b
	(6.2%)	(18.3%)	(12.5%)

1 Notes: Eggs were immersed in the extracts. aFor day 5, means within a column followed by the same letter are not significantly different according to a Kruskal–Wallis test with a Wilcoxon test for each pair of multiple comparisons (P ≤ 0.05). For day 7, means within a column followed by the same letter are not significantly different according to Tukey’s adjustment for multiple comparisons (P ≤ 0.05); bWater + K = water plus kanamycin monosulfate, which was added to all treatments except the water control;

cNumbers in parentheses are percentage decreases in treatments that significantly reduced % active J2 compared with the corresponding controls: the 0.5% DMSO control for 200 ug/ml, and the 1.0% DMSO control for 400 ug/ml.

Table 4.

Meloidogyne incognita second-stage juvenile (J2) activity and viability in methanolic extracts from roots and shoots of Festulolium lines FHCD0802 BUS 10-12 U6+ and FHCD0802 U6−.

	Day 1, % active J2		Day 2, % active J2		Day 3 rinsed, % viable J2
% DMSO in controls or µg/ml extract	Roots^a	Shoots	Roots	Shoots	Roots	Shoots
Water	89.2 a	89.2 ab	91.4 a	91.4 a	86.7 a	86.7 a
Water + K^b	86.2 ab	86.2 ab	91.4 ab	91.4 ab	88.4 a	88.4 a
0.5% DMSO	87.7 a	87.7 ab	90.5 ab	90.5 a	85.8 a	85.8 a
1.0% DMSO	88.3 a	88.3 ab	87.2 ab	87.2 abc	85.4 a	85.4 a
U6 E+ 200 µg/ml	82.8 ab	85.4 b	86.1 ab	88.8 abc	70.0 b	68.7 b
	–	–	–	–	(18.4%)	(19.9%)
U6 E− 200 µg/ml	78.7 b	84.4 b	84.0 ab	80.7 bc	68.9 b	66.2 b
	(10.3%)^c	–	–	(10.8%)	(19.7%)	(22.8%)
U6 E+ 400 µg/ml	90.4 a	90.9 ab	80.9 b	81.6 bc	70.0 b	71.2 b
	–	–	–	–	(18.0%)	(16.6%)
U6 E− 400 µg/ml	89.0 a	94.6 a	81.3 b	80.2 c	61.2 b	60.7 b
	–	–	–	–	(28.3%)	(28.9%)

1 Notes: Previously hatched J2 were immersed in the extracts. ^aMeans within a column followed by the same letter are not significantly different according to Tukey’s adjustment for multiple comparisons (P ≤ 0.05); ^bWater + K = water plus kanamycin monosulfate, which was added to all treatments except the water control; ^cNumbers in parentheses are percentage decreases in treatments that significantly reduced % active J2 compared with the corresponding controls: the 0.5% DMSO control for 200 ug/ml, and the 1.0% DMSO control for 400 ug/ml.

Table 5.

Plant vigor and Meloidogyne incognita population densities from Festulolium lines, plus and minus the endophytes U2 and U5, and from susceptible pepper plants in the greenhouse.

	Shoot fresh weight^a (g)		Root Fresh weight (g)		Root gall index^b		Total eggs per root system		Eggs per g of root
Plant and endophyte	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2
FHCF0802 U2 E−	33.0 a	71.4 a	98.1 aA	66.2 aAB	0	0.7 aB	817 aB	1,467 aB	9.7 aB	21.3 aB
FHCF0802 U2 E+	31.4 a	50.9 b	86.1 aAB	61.3 aB	0	1.0 aB	700 aB	0 aB	7.8 aB	0.0 aB
FHAC0802 U5 E−	29.3 a	70.3 a	41.4 aBC	63.3 aB	0	0.3 aB	817 aB	800 aB	19.5 aB	13.1 aB
FHAC0802 U5 E+	33.4 a	73.1 a	49.3 aABC	99.9 aA	0	0.3 aB	933 aB	1,733 aB	21.8 aB	16.1 aB
Pepper	NA	NA	14.1 C	15.7 C	25	25.0 A	225,108 A	104,000 A	15,975.0 A	6,239.7 A

1 Notes: aFor shoot fresh weight, root fresh weight, root gall index Trial 2 without pepper, total eggs per root system, and eggs per g of root Trial 1 and Trial 2 without pepper, means within a column followed by the same letter are not significantly different according to Tukey’s adjustment for multiple comparisons (P ≤ 0.05). For root gall index Trial 2 with pepper, and eggs per g of root Trial 2 with pepper, means within a column followed by the same letter are not significantly different according to a Kruskal–Wallis test with a Wilcoxon test for each pair of multiple comparisons (P ≤ 0.05). Lower case letters are for comparisons among Festulolium plants only. Upper case letters are for comparison among all plants, including pepper; broot gall indices follow Daulton and Nusbaum (1961). 0 = no galls, 1 = 1 to 4 galls, 5 = 5 to 25 galls, 10 = 26 to 100 galls and 25 = more than 100 galls.

Table 6.

Plant vigor and Meloidogyne incognita population densities from Festulolium lines, plus and minus the endophytes U6, U8, and U10, and from susceptible pepper plants in the greenhouse.

	Shoot fresh weight^a (g)		Root fresh weight (g)		Root gall index^b		Total eggs per root system		Eggs per g of root
Plant and endophyte	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2
FHCD0802 U6 E−	24.0 a	43.2 ab	16.1 aAB	34.7 abAB	6.7 aB	8.3 aB	10,533 aB	0 aB	500.0 aB	0.0 aB
FHCD0802 U6 E+	17.1 ab	33.9 ab	12.2 aAB	24.7 bBC	6.7 aB	5.0 aB	3,067 aB	0 aB	284.5 aB	0.0 aB
FHAB0802 U8 E−	19.9 ab	31.7 b	14.5 aAB	25.0 abBC	8.3 aA	0.0 aB	933 aB	0 aB	63.1 aB	0.0 aB
FHAB0802 U8 E+	11.7 ab	29.2 b	13.1 aAB	17.4 bBC	3.3 aB	6.7 aB	933 aB	53 aB	71.2 aB	3.0 aB
FHCD0802 U10 E−	18.1 ab	51.5 a	14.0 aAB	47.3 aA	6.7 aB	6.7 aB	1,333 aB	40 aB	95.3 aB	1.0 aB
FHCD0802 U10 E+	6.5 b	29.7 b	4.0 aB	22.2 bBC	5.3 aB	1.7 aB	533 aB	13 aB	803.2 aB	0.7 aB
Pepper	NA	NA	17.0 A	13.5 C	25.0 A	25.0 A	466,933 A	119,333 A	27,644.3 A	8,552.8 A

1 Notes: aFor shoot fresh weight, root fresh weight, root gall index Trial 2, and eggs per g of root Trial 1 with pepper, means within a column followed by the same letter are not significantly different according to Tukey’s adjustment for multiple comparisons (P ≤ 0.05). For root gall index Trial 1, total eggs per root system, and eggs per g of root Trial 1 without pepper and Trial 2 with and without pepper, means within a column followed by the same letter are not significantly different according to a Kruskal–Wallis test with a Wilcoxon test for each pair of multiple comparisons (P ≤ 0.05). Lower case letters are for comparisons among Festulolium plants only. Upper case letters are for comparison among all plants, including pepper; broot gall indices follow Daulton and Nusbaum (1961). 0 = no galls, 1 = 1 to 4 galls, 5 = 5 to 25 galls, 10 = 26 to 100 galls and 25 = more than 100 galls.

Table 7.

Meloidogyne incognita population densities on pepper in soil that was previously planted to Festulolium with or without a U2 or U5 endophyte, to susceptible pepper, or left fallow in the greenhouse.

	Root fresh weight^a (g)		Root gall index^b		Total eggs per root system		Eggs per g of root
Previous treatment: Fallow, Festulolium line and endophyte, or pepper	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2
Fallow	6.8 ab	20.3 ab	4.3 b	0.5 c	4,550 b	200 c	679.8 b	9.2 c
FHCF0802 U2 E−	5.2 b	22.5 ab	22.5 a	25.0 ab	58,450 a	135,200 ab	10,316.0 a	5,047.7 ab
FHCF0802 U2 E+	6.7 ab	23.5 ab	17.5 ab	11.7 bc	37,625 a	10,267 bc	5,382.0 a	613.0 bc
FHAC0802 U5 E−	6.4 ab	19.5 ab	13.3 ab	18.3 ab	34,650 a	18,267 b	5,264.2 a	823.7 b
FHAC0802 U5 E+	7.3 a	25.4 a	7.2 b	3.3 c	21,700 ab	533 bc	3,045.7 ab	18.3 bc
Pepper	2.6 c	11.7 b	16.0 ab	25.0 a	17,010 a	207,467 a	6,293.4 a	16,420.5 a

1 Notes: aFor root fresh weight and root gall index, means within a column followed by the same letter are not significantly different according to Tukey’s adjustment for multiple comparisons (P ≤ 0.05). For total eggs per root system and eggs per g of root, means within a column followed by the same letter are not significantly different according to a Kruskal–Wallis test with a Wilcoxon test for each pair of multiple comparisons (P ≤ 0.05); broot gall indices follow Daulton and Nusbaum (1961). 0 = no galls, 1 = 1 to 4 galls, 5 = 5 to 25 galls, 10 = 26 to 100 galls, and 25 = more than 100 galls.

Table 8.

Meloidogyne incognita population densities on pepper in soil that was previously planted to Festulolium with or without a U6, U8, or U10 endophyte, to pepper, or left fallow in the greenhouse.

	Root fresh weight^a (g)		Root gall index^b		Total eggs per root system		Eggs per g of root
Previous treatment: Fallow, Festulolium line and endophyte, or pepper	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2	Trial 1	Trial 2
Fallow	6.4 a	7.8 bc	8.3 b	0.8 c	3 c	3,233 c	0.5 b	533.5 b
FHCD0802 U6 E−	6.3 a	14.1 a	20.0 a	18.3 ab	193,600 ab	1,333 bcd	33,590.0 a	81.0 bc
FHCD0802 U6 E+	6.1 a	11.8 ab	25.0 a	15.0 ab	403,467 a	12,000 bd	56,056.7 a	1,105.0 bc
FHAB0802 U8 E−	5.3 a	10.1 abc	25.0 a	0.0 bc	87,200 ab	533 d	21,668.7 a	73.0 bc
FHAB0802 U8 E+	5.6 a	10.6 abc	25.0 a	0.0 bc	37,333 ab	1,333 d	6,400.0 a	123.0 c
FHCD0802 U10 E−	5.8 a	10.5 abc	25.0 a	18.3 ab	47,200 ab	5,067 bcd	8,137.7 a	485.3 bc
FHCD0802 U10 E+	6.6 a	11.1 ab	25.0 a	0.0 bc	35,733 ab	800 d	5,269.7 a	78.7 c
Pepper	2.4 b	5.5 c	25.0 a	25.0 a	10,800 b	100,033 a	5,301.5 a	17,842.3 a

1 Notes: aFor root fresh weight, means within a column followed by the same letter are not significantly different according to Tukey’s adjustment for multiple comparisons (P ≤ 0.05). For root gall index, total eggs per root system, and eggs per g of root, means within a column followed by the same letter are not significantly different according to a Kruskal–Wallis test with a Wilcoxon test for each pair of multiple comparisons (P ≤ 0.05); broot gall indices follow Daulton and Nusbaum (1961). 0 = no galls, 1 = 1 to 4 galls, 5 = 5 to 25 galls, 10 = 26 to 100 galls, and 25 = more than 100 galls.

Table 9.

Host status of grass cultivar/endophyte associations to Meloidogyne spp. Grasses: tall fescue (Schedonorus arundinaceus); Italian ryegrass (Festuca perennis; syn. Lolium multiflorum).

Tall Fescue Cultivar (Endophyte)	M. arenaria Peanut root-knot nematode	M. hapla Northern root-knot nematode	M. incognita Southern root-knot nematode	M. javanica Javanese root-knot nematode	M. marylandi Maryland root-knot nematode
Bulldog 51 (E+ toxic)^a	Host^b	–	Poor Host^b	Host^b	–
Jesup (Wild Type) (E+ toxic)	–	–	Nonhost^b	–	–
Jesup (Max-Q) (E+ nontoxic AR542)	Host^b	Nonhost^b	Nonhost^b	Poor Host^b	–
Jesup (E− no endophyte)	–	–	Nonhost^b	–	–
Georgia 5 (E+ toxic)	–	–	Nonhost^b	–	–
Kentucky 31 (E+)	–	–	Host^c	–	Poor Host^d
Kentucky 31 (E− no endophyte)	–	–	Host^c	–	Host^d
Genotype GA 1987 (E+)	–	–	–	–	Host^e
Genotype GA 1987 (E−)	–	–	–	–	Poor host^e
Genotype GA 2109 (E+)	–	–	–	–	Poor host^e
Genotype GA 2109 (E−)	–	–	–	–	Poor host^e
Genotype GA 2125 (E+)	–	–	–	–	Poor host^e
Genotype GA 2125 (E−)	–	–	–	–	Poor host^e
Genotype GA 3084 (E+)	–	–	–	–	Poor host^e
Genotype GA 3084 (E−)	–	–	–	–	Poor host^e
Genotype GA87-122 (E+)	–	–	–	–	Poor host^f
Genotype GA87-122 (E−)	–	–	–	–	Host^f
Italian ryegrass Cultivar (Endophyte)
Bishamon (E+)	Host^g	–	Host^g	–	–
Bishamon (E−)	Host^g	–	Host^g	–	–
JFIR-18 (E+)	Host^g	–	Host^g	–	–
JFIR-18 (E−)	Host^g	–	Host^g	–	–

1 Notes: aDescribed as toxic (= toxic to mammals); endophyte produces ergot alkaloids. Nontoxic=endophyte does not produce ergot alkaloids; bNyczepir and Meyer (2010); cJia et al. (2013); dKimmons et al. (1990); eKirkpatrick et al. (1990). Although listed in the paper as M. graminis, the nematode was likely M. marylandi (personal communication, T. Kirkpatrick, 2019); fElmi et al. (2000); gUesugi et al. (2014).

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DOI: https://doi.org/10.21307/jofnem-2020-076 | Journal eISSN: 2640-396X | Journal ISSN: 0022-300X

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Language: English

Page range: 1 - 16

Published online: Jul 28, 2020

Published in print: Jan 1, 2020

Published by: Society of Nematologists, Inc.

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Publication frequency: 1 issue per year

Keywords:

Festuca,

Lolium,

Meloidogyne incognita,

Nematode host status,

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© 2020 Susan L. F. Meyer, Brian J. Patchett, Timothy J. Gillanders, Mihail R. Kantor, Patricia Timper, Margaret H. MacDonald, published by Society of Nematologists, Inc.
This work is licensed under the Creative Commons Attribution 4.0 License.

Volume 52 (2020): Issue 1 (January 2020)