Genome-wide association study identifies favorable SNP alleles and candidate genes for frost tolerance in pea

Beji, Sana; Fontaine, Véronique; Devaux, Rosemonde; Thomas, Martine; Negro, Sandra Silvia; Bahrman, Nasser; Siol, Mathieu; Aubert, Grégoire; Burstin, Judith; Hilbert, Jean-Louis; Delbreil, Bruno; Lejeune-Hénaut, Isabelle

doi:10.1186/s12864-020-06928-w

BMC Genomics

Table 3 Significant associations detected in the association mapping collection (363 accessions) for the five observed traits

From: Genome-wide association study identifies favorable SNP alleles and candidate genes for frost tolerance in pea

Associated marker	Genetic map ^a		Physical map ^b		Associated trait	-log₁₀ (p)	Minor allele (MAF) ^c	Allelic effect ^d	SE ^e	Favorable allele	Allele of reference accessions
Associated marker	Linkage group	Genetic position (cM)	Chromosome	Physical position (bp)	Associated trait	-log₁₀ (p)	Minor allele (MAF) ^c	Allelic effect ^d	SE ^e	Favorable allele	Champagne	Térèse	China	Caméor
PsCam020765_11567_1428	I	47.5	2	160,946,678	FD_Field_date1	5.57	B (0.13)	0.18	0.04	A	AA	BB	AA	AA
PsCam043698_27686_2011	II	20.5	6	29,326,358	FD_CC	5.45	B (0.39)	0.18	0.04	A	AA	BB	AA	AA
PsCam049061_31705_537	III	131.1	5	566,158,491	FD_CC	5.55	B (0.50)	−0.29	0.06	B	AA	BB	AA	BB
PsCam035617_20792_637	III	132	5	566,953,569	FD_CC	6.63	A (0.50)	−0.37	0.07	A	BB	AA	BB	AA
PsCam035617_20792_637	III	132	5	566,953,569	FD_Field_date1	5.47	A (0.50)	−0.31	0.07	A	BB	AA	BB	AA
PsCam037922_22979_691	III	132.1	5	567,367,194	FD_CC	6.63	A (0.50)	−0.37	0.07	A	BB	AA	BB	AA
PsCam037922_22979_691	III	132.1	5	567,367,194	FD_Field_date1	5.47	A (0.50)	−0.31	0.07	A	BB	AA	BB	AA
PsCam051352_33858_733	V	53.6	scaffold01940	189,591	FD_Field_date4	7.29	A (0.25)	−0.27	0.05	A	AA	BB	BB	AA
PsCam048068_30823_2326	V	56.9	3	181,347,340	FD_Field_date4	6.21	B (0.33)	−0.26	0.05	B	BB	AA	BB	AA
PsCam002670_2123_708	V	58.6	3	184,294,454	FD_Field_date4	6.99	A (0.19)	−0.23	0.04	A	AA	BB	BB	BB
PsCam051635_34107_368	V	58.6	3	184,298,068	FD_Field_date4	9.21	A (0.27)	−0.33	0.05	A	AA	BB	BB	BB
PsCam011361_7735_182	V	60.2	3	189,446,769	FD_Field_date4	5.88	A (0.26)	−0.25	0.05	A	AA	BB	BB	BB
PsCam012913_8715_718	V	60.2	3	187,888,138	FD_Field_date4	5.43	A (0.32)	−0.22	0.05	A	AA	BB	AA	BB
PsCam049838_32453_1430	V	60.2	3	189,010,331	FD_Field_date4	7.17	B (0.28)	−0.26	0.05	B	BB	AA	BB	AA
PsCam042222_26315_1205	V	61	3	193,904,545	FD_Field_date4	10.01	A (0.24)	−0.38	0.06	A	AA	BB	BB	BB
PsCam021402_12023_752	VI	41.4	1	119,086,683	FD_Field_date4	5.84	A (0.21)	−0.23	0.05	A	AA	BB	BB	BB
PsCam043553_27552_265	VI	43	1	124,617,110	FD_Field_date4	5.95	A (0.22)	−0.25	0.05	A	AA	BB	BB	BB
PsCam022275_12527_210	VI	47.4	1	167,098,866	FD_CC	6.21	B (0.23)	−0.33	0.06	B	BB	AA	AA	AA
					FD_Field_date1	5.64	B (0.23)	−0.29	0.06
					FD_Field_date4	6.86	B (0.23)	−0.27	0.05
PsCam003541_2731_574	VI	48	1	165,049,951	FD_CC	6.51	A (0.44)	0.21	0.04	B	BB	BB	AA	BB
PsCam050834_33394_133	VI	48.5	1	165,743,845	FD_CC	5.35	A (0.33)	−0.25	0.05	A	AA	BB	AA	BB
PsCam001662_1375_798	VI	49.1	1	168,461,782	FD_CC	7.38	A (0.31)	−0.35	0.06	A	AA	BB	AA	BB
PsCam001662_1375_798	VI	49.1	1	168,461,782	FD_Field_date4	6.08	A (0.31)	−0.24	0.05	A	AA	BB	AA	BB
PsCam043847_27818_181	VI	49.1	1	175,268,097	FD_CC	5.90	A (0.27)	−0.29	0.06	A	AA	BB	AA	BB
PsCam045419_29091_815	VI	49.1	1	169,979,594	FD_CC	7.57	B (0.37)	−0.24	0.04	B	BB	AA	BB	AA
PsCam048404_31138_2325	VI	49.1	1	170,956,086	FD_CC	6.02	B (0.31)	−0.30	0.06	B	BB	AA	BB	AA
PsCam004890_3696_1580	VI	49.1	1	181,902,508	FD_Field_date4	5.82	A (0.22)	−0.24	0.05	A	AA	BB	BB	BB
PsCam023246_13111_1125	VI	49.1	1	167,654,791	FD_Field_date4	5.40	B (0.21)	−0.25	0.05	B	BB	AA	AA	AA
PsCam037082_22189_1302	VI	49.1	1	181,965,322	FD_Field_date4	5.40	B (0.22)	−0.23	0.05	B	BB	AA	AA	AA
PsCam053556_35439_228	VI	49.1	1	166,361,064	FD_Field_date4	5.39	B (0.31)	−0.21	0.04	B	BB	AA	BB	AA
PsCam007060_5248_2156	VI	50.1	1	179,745,943	FD_CC	7.66	B (0.40)	0.22	0.04	A	AA	AA	AA	BB
PsCam026381_15234_450	VI	50.1	1	178,695,180	FD_CC	6.33	B (0.47)	0.21	0.04	A	AA	AA	BB	BB
PsCam037879_22937_948	VI	50.1	1	178,713,424	FD_CC	9.90	A (0.43)	0.26	0.04	B	BB	BB	BB	AA
PsCam001302_1089_1249	VI	50.2	1	182,819,711	FD_CC	6.50	B (0.46)	−0.22	0.04	B	BB	BB	AA	AA
PsCam003337_2589_220	VI	50.2	1	180,428,730	FD_CC	7.34	A (0.39)	0.22	0.04	B	BB	BB	BB	AA
PsCam037603_22679_2024	VI	50.2	1	180,042,543	FD_CC	7.59	A (0.38)	0.22	0.04	B	BB	BB	BB	AA
PsCam040539_25267_719	VI	50.2	1	181,440,108	FD_CC	7.59	A (0.38)	0.22	0.04	B	BB	BB	BB	AA
PsCam035398_20586_1094	VI	50.6	1	194,261,395	FD_CC	7.63	B (0.50)	−0.25	0.04	B	BB	AA	BB	AA
PsCam039054_24037_586	VI	50.6	1	210,266,228	FD_CC	6.30	B (0.41)	0.21	0.04	A	AA	AA	AA	BB
PsCam049925_32537_2703	VI	50.7	1	194,874,039	FD_CC	6.57	B (0.41)	0.22	0.04	A	AA	AA	AA	BB
PsCam038477_23510_469	VI	50.8	1	194,779,560	FD_CC	7.67	B (0.39)	−0.27	0.05	B	BB	AA	BB	AA
PsCam001148_968_692	VI	51.1	1	218,959,228	FD_CC	6.06	B (0.50)	0.22	0.04	A	AA	AA	BB	AA
PsCam006586_4888_245	VI	51.1	1	218,476,070	FD_CC	6.00	A (0.41)	0.20	0.04	B	BB	BB	AA	BB
PsCam017327_10745_93	VI	51.1	1	208,681,226	FD_CC	8.40	B (0.48)	−0.27	0.04	B	BB	BB	BB	AA
PsCam020872_11644_1756	VI	51.1	1	217,751,686	FD_CC	7.31	B (0.45)	0.23	0.04	A	AA	AA	BB	AA
PsCam025448_14564_2314	VI	51.1	1	218,939,803	FD_CC	6.08	A (0.29)	−0.22	0.04	A	AA	BB	BB	AA
PsCam033562_19160_307	VI	51.1	1	217,753,744	FD_CC	6.04	A (0.48)	0.21	0.04	B	BB	BB	AA	BB
PsCam036704_21832_970	VI	51.1	7	404,463,902	FD_CC	7.12	B (0.48)	0.22	0.04	A	AA	AA	BB	AA
PsCam038677_23691_325	VI	51.1	1	221,377,153	FD_CC	6.59	B (0.43)	0.20	0.04	A	AA	AA	BB	AA
PsCam044418_28295_579	VI	51.1	1	217,447,863	FD_CC	6.61	A (0.41)	0.21	0.04	B	BB	BB	AA	BB
PsCam052151_34533_410	VI	51.1	1	216,779,912	FD_CC	6.16	A (0.47)	0.21	0.04	B	BB	BB	AA	BB
PsCam053189_35238_569	VI	51.1	1	216,188,812	FD_CC	7.30	B (0.49)	0.23	0.04	A	AA	AA	BB	AA
PsCam042568_26621_42	VI	51.1	1	213,838,599	FD_Field_date4	5.43	A (0.21)	−0.25	0.05	A	AA	BB	BB	BB
PsCam035356_20546_778	VI	52.5	1	221,502,038	FD_CC	5.99	B (0.43)	0.20	0.04	A	AA	AA	BB	AA
PsCam040326_25099_1923	VI	52.5	1	226,457,822	FD_CC	5.91	A (0.38)	0.20	0.04	B	BB	BB	AA	BB
PsCam011774_8038_200	VI	52.8	1	232,110,795	FD_CC	6.76	A (0.49)	−0.23	0.04	A	AA	BB	BB	AA
PsCam023852_13541_264	VI	52.8	1	232,209,522	FD_CC	6.71	B (0.46)	−0.24	0.04	B	BB	AA	AA	BB
PsCam026055_15000_192	VI	52.8	1	228,344,153	FD_CC	5.70	B (0.44)	−0.22	0.04	B	BB	AA	AA	BB
PsCam001108_940_48	VII	72.9	7	338,172,762	FD_Field_date2	5.74	B (0.48)	0.20	0.04	A	BB	AA	AA	AA
PsCam001108_940_48	VII	72.9	7	338,172,762	FD_Field_date3	5.34	B (0.48)	0.21	0.05	A	BB	AA	AA	AA
PsCam050827_33387_242	VII	82.4	scaffold02790	184,253	FD_Field_date2	6.27	B (0.21)	0.21	0.04	A	AA	AA	AA	AA
PsCam037927_22984_97	VII	82.5	7	364,561,668	FD_Field_date2	5.40	B (0.41)	0.19	0.04	A	BB	AA	AA	BB
PsCam038378_23415_721	VII	86.4	7	416,077,744	FD_CC	6.18	A (0.46)	0.22	0.04	B	BB	BB	BB	AA
PsCam042427_26489_524	VII	87.1	7	417,288,899	FD_CC	5.67	B (0.41)	0.20	0.04	A	AA	AA	AA	BB
PsCam000301_265_1519	VII	87.9	7	424,418,432	FD_Field_date2	7.41	B (0.19)	0.23	0.04	A	AA	AA	AA	BB
PsCam000301_265_1519	VII	87.9	7	424,418,432	FD_Field_date3	5.72	B (0.19)	0.22	0.05	A	AA	AA	AA	BB
PsCam045010_28743_3365	VII	88	scaffold02266	42,102	FD_Field_date2	5.73	B (0.21)	0.20	0.04	A	AA	AA	AA	BB
PsCam004928_3732_3087	VII	89.3	7	430,325,609	FD_Field_date2	7.46	B (0.28)	0.25	0.04	A	AA	AA	AA	AA
PsCam004928_3732_3087	VII	89.3	7	430,325,609	FD_Field_date3	5.40	B (0.28)	0.24	0.05	A	AA	AA	AA	AA

Traits are coded as described in Table 1. For each associated SNP, genetic and physical positions are indicated. ^a: Linkage groups are named from I to VII and the genetic position is indicated in cM Haldane following the consensus map from Tayeh et al. [36]. ^b: Physical marker position results from the projection of the marker onto the Pisum sativum v.1a genome JBrowse available at https://urgi.versailles.inra.fr/Species/Pisum [39]. Chromosomes are named in consecutive numerical order from 1 to 7 and physical positions are indicated in bp. Markers which are not assigned to one of the seven chromosomes are represented by their physical position on unanchored scaffolds. Significance threshold of the marker-trait association is -log₁₀ (p) > 5.33 as described in the Material and Methods section. For each associated SNP, the allelic effect of the minor allele as well as the favorable allele are listed. ^c: Minor allele frequency; ^d: Allele effect of the minor allele. ^e: standard error of the allelic effect. Alleles of four cultivars which are the progenitors of bi-parental mapping populations for frost tolerance are listed to illustrate contrasted genotypes for this trait: Champagne and China (frost tolerant), Térèse and Caméor (frost sensitive)

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