玉米盐胁迫相关性状全基因组关联分析及候选基因预测

doi:10.16288/j.yczz.21-298

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Hereditas(Beijing) ›› 2021, Vol. 43 ›› Issue (12): 1159-1169.doi: 10.16288/j.yczz.21-298

• Research Article • Previous Articles Next Articles

Genome-wide association study and candidate gene prediction of salt tolerance related traits in maize

Tingyu Shan(), Wen Shi, Yiting Wang, Ziyi Cao, Baohua Wang, Hui Fang()

Ministry of Agricultural Scientific Observing and Experimental Station of Maize in Plain Area of Southern Region, School of Life Sciences, Nantong University, Nantong 226019, China

Received:2021-08-13 Revised:2021-10-02 Online:2021-12-20 Published:2021-12-07
Contact: Fang Hui E-mail:shan_0822@126.com;fanghui8912@126.com
Supported by:
Supported by the Science and Technology Project of Nantong City, China(MS22020033);Talent Introduction Project of Nantong University No(135420609055)

Abstract

Abstract:

Salt stress is an important factor that affects maize yield. In order to explore the genetic basis of salt tolerance in maize, a genome-wide association study (GWAS) using the mixed liner model was conducted on 150 maize inbred lines with rich genetic background and 34,342 polymorphism SNP markers. A total of 8 independent loci were identified that significantly associated with salt-tolerance traits, among which 3 loci were significantly associated with withering degree on chromosomes 4 and 9; and the remaining 5 loci were significantly associated with plant height change rate on chromosomes 1, 2, 3 and 6. Eleven candidate genes were identified according to the gene expression data under salt stress; and functional annotations verified 7 of them to be significantly up-regulated under salt stress by qRT-PCR. These findings lay a foundation for understanding the mechanism(s) of maize salt tolerance and provide new target genes for the breeding of maize salt tolerance germplasm.

Key words: maize, salt tolerance, mixed liner model, genome-wide association study

Tingyu Shan, Wen Shi, Yiting Wang, Ziyi Cao, Baohua Wang, Hui Fang. Genome-wide association study and candidate gene prediction of salt tolerance related traits in maize[J]. Hereditas(Beijing), 2021, 43(12): 1159-1169.

Figures/Tables 14

Fig. 1

Fig. 2

Table 1

Fig. 3

Table 2

Table 3

Fig. 4

Fig. 5

Table 4

Supplementary Table 1

Supplementary Table 2

Supplementary Table 3

Phenotypic results of salt stress-related traits"

家系名称	T1	T2	T3	T4
764	4	0.106685807	0.859905959	0.775090325
779	3.666666667	0.053892216	0.441441441	0.034965035
904	3.333333333	0.120395688	0.885410628	0.525030525
912	3.75	-0.022568998	0.640350877	0.20970266
2369	4	0.188785703	0.785634119	0.527058824
11430	3.333333333	0.138089758	0.487804878	0.385481852
4676A	2	0.019224102	0.688906798	0.130612245
6F629	5	0.065575558	0.703703704	-0.715789474
78002A	4.5	0.161691542	0.5	-0.015384615
78371A	2.666666667	0.087169299	0.450910931	-0.247563353
78551S	5	0.332941696	0.834848485	0.55
83IBI3	3.5	0.23180624	0.75049891	-0.30625
87916W	5	0.139334378	0.783488028	-0.195845697
A635	5	0.182547395	0.720695971	0.268096515
B14	4.666666667	-0.421686747	0.363636364	-1.133757962
B14A	4.5	0.301216743	0.831049398	0.715843489
B37	3	0.136442918	0.8255563	0.142857143
B47	5	0.309312793	0.871871872	0.490701001
C103	4	0.558739226	0.910714286	0.464174455
CO109	2	-0.076696165	0	0.07826087
CR14	4.333333333	0.014563107	0.52173913	0.536516854
E8501	3	0.216734631	0.827926421	0.843537415
F42	2.666666667	0.134222222	0.5	0.093406593
FAPW	4	0.286407767	0.636363636	0.203597122
FR19	5	0.310602547	0.875838947	0.338830585
H93	5	0.053082505	0.692640693	-0.528767123
HB8229	1.666666667	-0.166666667	0.272727273	0.273139746
IB02	5	0.382641225	0.558823529	0.389112903
IBB15	2.666666667	0.125596897	0.792174797	0.340588988
IBO14	5	0.310928226	0.829650504	0.083916084
L135	5	-0.015375964	0.298611111	-0.00538358
L139	2	0.094623146	0.728282828	0.07106599
L317	4.666666667	0.432276531	0.873738254	0.348484848
LH128	3	-0.477574144	0.741428571	0.484827586
LH132	4	0.180683002	0.755934783	0.773415133
LH143	3.333333333	-0.285917994	0.468148148	0.063334983
LH145	3.666666667	-0.128747795	0.296296296	-0.339694656
LH146HT	5	0.031914894	0.6	0.158371041
LH149	5	-0.81443299	0.25	-0.047619048
LH160	3	0.143435352	0.774744974	0.776025237
LH162	4	-0.198924699	0.192639805	0.679364669
LH163	3	-0.160241915	0.631410256	0.074198988
LH164	4	0.366197183	0.95	0.053254438
LH196	2	0.150510204	0.5	0.247654784
LH197	3	0.071724138	0.613636364	-0.625
LH202	2.666666667	-0.289041096	0.037037037	0.263665595
LH204	4.25	0.250292071	0.841452991	0.285356696
LH205	5	-0.149584076	0.919309524	0.807927812
LH213	4	0.155	0.069767442	0.605
LH214	4	0.146307858	0.75870936	0.356514788
LH216	3	0.08213168	0.594179894	0.272829763
LH220HT	2.75	0.320799608	0.79386883	0.482022472
LH222	3.75	0.250100281	0.704426129	-0.047038328
LH39	4	0.232224104	0.806684905	0.45472973
LH52	3	0.191662197	0.897622655	0.853852481
LH54	3.75	0.20716033	0.803333221	0.615072464
LH57	5	-0.013888889	0.476190476	0.363538296
LH61	4.8	0.22531233	0.718266254	-0.297577855
LH74	4	0.091427566	0.807241965	0.617501166
LH82	3	0.075389408	0.691056911	0.345581802
LH93	3	0.3253386	0.874730053	0.645687646
LP5	5	0.392215722	0.767102397	-0.051948052
MBPM	4.5	0.429179416	0.906234289	0.627483444
MBSJ	3	0.070597856	0.176470588	0.210869565
MBST	2	0.031718062	0.496296296	0.191637631
Mo22	3.75	-0.011951503	0.79111927	0.626065341
NC250	5	0.068195561	0.81547619	-0.145363409
ND203	3.5	0.034778671	0.526195286	-0.279346211
NQ508	4	-0.221556886	-1.058141026	0.169768754
NS501	4	0.182549203	0.558760684	-0.131880734
NS701	3	-0.392568659	0.148148148	0.355339806
Oh40B	5	-0.009803922	0.428571429	0.081451061
OH7B	3.5	0.177205024	0.63962704	0.224550898
P737M20	2.333333333	0.141843972	0.333333333	0.210884354
Pa91	2	0.034689864	0.808045815	0.723135146
PB80	4.333333333	0.161861037	0.693253923	0.165021157
PF010	3.333333333	0.309720548	0.860636507	0.557239057
PHBA6	3	-0.038989439	0.388678052	-0.830548926
PHG29	3.333333333	0.065765251	0.871539081	0.74143057
PHG35	4.666666667	0.293120097	0.923564127	0.862402512
PHG39	5	0.114242424	-0.545079365	0.283173077
PHG47	3	0.133514678	0.92	0.830970776
PHG50	2	0.2125746	0.869800202	0.8170164
PHG71	4	0.281727747	0.875491259	0.774668813
PHG72	5	0.40382879	0.951678788	0.847798341
PHG83	2.5	-0.325203252	-0.151515152	-1.230769231
PHG84	5	0.470915549	0.924074074	0.836134454
PHG86	3	0.063305513	0.799387904	0.739177883
PHGG7	3	0.064839051	0.880388466	0.801129332
PHH93	4	0.075818696	0.73994832	0.938946046
PHHH9	3.666666667	0.186025829	0.841795255	0.851485149
PHJ40	4.666666667	0.016144349	0.515789474	0.016645327
PHJ70	4	0.182412791	0.658227848	0.370417193
PHJ75	2.666666667	0.202660478	0.771780405	0.710249474
PHJ90	2	0.105318062	0.785738301	0.74165577
PHK05	3.666666667	-0.064676617	-0.179487179	-0.730200174
PHK29	3	0.125299248	0.778988805	0.772440526
PHK35	5	0.252361057	0.929857143	0.849577532
PHK42	2	-0.086715867	0.130434783	0.305232558
PHK76	4.5	0.202912215	0.310810811	0.05
PHKE6	3.333333333	-0.041915065	0.533501604	0.124
PHM10	4.333333333	0.025943396	0.481481481	0.06446281
PHM57	2.666666667	0.38240269	0.851551971	0.860177467
PHM81	3.666666667	-0.221052632	-0.107142857	0.312684366
PHN11	4	0.2244816	0.719628647	0.196078431
PHN29	5	0.263157895	0.555555556	0.944954128
PHN47	4.25	0.024830793	0.739251768	0.164233577
PHN66	4	0.139673354	0.742966277	0.021935484
PHN73	4	0.020422018	0.811269556	0.743728068
PHN82	4.5	0.049443442	0.802449965	0.597969543
PHP02	4	0.035364483	0.602286325	0.484480432
PHP55	5	0.261301942	0.785714286	0.31686747
PHP60	4.5	0.009009009	0.44	0.050179211
PHP85	5	0.237179487	0.403508772	0.212627669
PHR25	3	0.098412698	0.229166667	0.261989343
PHR32	4	0.114851636	0.912760137	0.488294314
PHR36	4	0.27199986	0.838235294	0.115
PHR47	5	0.281074811	0.5875	0.427966102
PHR55	4	-0.072343744	0.607460317	-1.69001387
PHR58	4	-0.234189084	0.837209302	0.417682927
PHR62	4.333333333	-0.015039405	0.723585859	0.092957746
PHR63	3	-0.025642716	0.879562948	0.76727909
PHT10	3	0.036237933	0.866034337	0.807460176
PHT22	3.333333333	0.208751022	0.742037037	0.746268657
PHT55	5	0.210235665	0.959651515	0.928606153
PHT60	3.666666667	0.273846154	0.49122807	-0.107317073
PHV07	3	0.059171598	0.203389831	-0.100628931
PHV37	2	0.063039724	0.479166667	-0.169934641
PHV53	5	0.071045068	0.946530604	0.866765496
PHV78	5	-0.101263146	0.565121136	-0.078014184
PHVA9	3.25	0.190359348	0.806177156	0.805031447
PHW03	2.333333333	0.00662121	0.318347271	-0.342763874
PHW17	5	-0.104384214	0.815278788	0.69679773
PHW20	4	0.069364162	0.5125	0.129181084
PHW30	5	-0.324631794	0.698446637	0.521840614
PHW51	4	0.132500019	0.764473304	0.645142637
PHW52	5	0.012268182	0.137931034	0.176470588
PHWG5	3	-0.082323159	0.665372199	-0.05483871
PHZ51	3	0.139534884	0.5625	0.023224044
POP-N-EAT	2.25	-0.03435569	0.650768766	0.71042471
Q381	4.333333333	0.093844601	0.378787879	0.236961451
RS710	3.25	0.246142459	0.841076856	0.850202429
SG17	3.666666667	0.279799616	0.861968465	0.529527559
T226	5	0.195014617	0.735802728	-0.318181818
T8	2.666666667	0.122820737	0.689078642	0.212806026
Va35	2	0.178753558	0.898576185	0.783600802
W22	4.333333333	0.261864034	0.068783069	-0.426829268
W8304	4.666666667	0.114802673	0.757346491	-0.010791367
W8555	3.333333333	0.197577587	0.522999223	-0.91321499
WIL903	3.333333333	0.243623993	0.626071044	0.033678756

Supplementary Table 3

Supplementary Table 4

All genes within the 50 Kb range before and after the significant SNP locus"

性状	显著SNP	染色体	start	end	候选基因_V2	候选基因_V4	注释
T1	PZE-104036105	4	47199131	47199937	GRMZM2G325580	Zm00001d049865	CASP-like protein
T1	SYN16455	4	239623748	239627091	GRMZM2G074423	Zm00001d054004	plant-specific domain tigr01589 family protein
T1	SYN16455	4	239627275	239630488	GRMZM2G074414	Zm00001d054005	biotinyl-lipoyl domain- containing protein
T1	SYN16455	4	239630746	239640417	GRMZM2G074278	Zm00001d054005	ap-3 complex subunit mu-1-like
T1	SYN16455	4	239640750	239641632	GRMZM2G074252	Zm00001d054006	hypothetical protein SORBIDRAFT_04g001625
T1	SYN16455	4	239643193	239651050	GRMZM2G074015	Zm00001d054008	mevalonate kinase
T1	SYN38269	9	136552200	136555676	GRMZM2G006429	Zm00001d047679	probable protein phosphatase 2c 5-like
T1	SYN38269	9	136558046	136561365	GRMZM2G006714	Zm00001d047680	calmodulin-binding protein
T1	SYN38269	9	136572037	136574076	GRMZM2G306482	Zm00001d047681	pentatricopeptide repeat- containing protein at5g50990-like
T1	SYN38269	9	136576621	136577373	GRMZM2G006830	Zm00001d047681	protein cobra
T1	SYN38269	9	136583501	136589780	GRMZM2G006884	Zm00001d047682	--NA--
T1	SYN38269	9	136615573	136620806	GRMZM5G830983	Zm00001d047683	udp-glucose 4-epimerase
T2	SYNGENTA5755	1	212166415	212168249	GRMZM2G067235	Zm00001d032164	hypothetical protein
T2	SYNGENTA5755	1	212191637	212196339	GRMZM2G067067	Zm00001d032165	Defective in cullin neddylation protein
T2	SYNGENTA5755	1	212287664	212305641	GRMZM2G160927	Zm00001d032166	DUF1336 domain-containing protein
T2	SYNGENTA5755	1	212332408	212358537	GRMZM2G005955	Zm00001d032170	lipid binding
T2	PZE-101169962	1	213230607	213233044	GRMZM2G117193	Zm00001d032190	MYB family transcription factor
T2	PZE-101169962	1	213309345	213314586	GRMZM2G031677	Zm00001d032192	ap-3 complex subunit mu-1-like
T2	SYN1142	2	9085071	9088878	GRMZM2G084046	Zm00001d002274	dna binding
T2	SYN1142	2	9114721	9126810	GRMZM2G084181	Zm00001d002275	abc transporter c family member 2-like
T2	SYN1142	2	9127513	9128809	GRMZM2G084325	Zm00001d002276	5a2 protein precursor
T2	SYN1142	2	9128588	9133414	GRMZM2G383122	Zm00001d002277	Ubiquitin-like domain- containing protein
T2	PHM13742.5	3	215169901	215182117	GRMZM2G088436	Zm00001d044089	rna polymerase sigma factor-like
T2	PHM13742.5	3	215207099	215211653	GRMZM2G088397	Zm00001d044090	5'-deoxynucleotidase
T2	PHM13742.5	3	215213789	215219139	GRMZM2G088299	Zm00001d044091	serine threonine-protein kinase ht1-like
T2	PZE-106065133	6	117370662	117372555	GRMZM2G012717	Zm00001d037327	zinc finger
T2	PZE-106065133	6	117452361	117454400	GRMZM2G168304	Zm00001d037328	3-ketoacyl-CoA synthase
T2	PZE-106065133	6	117595563	117599517	GRMZM2G382711	Zm00001d037329	uncharacterized protein

Supplementary Table 4

Supplementary Fig. 1

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亲缘关系系数	数量^a	百分比(%)
0~0.2	6085	54.47
0.2~0.4	3422	30.63
0.4~0.6	966	8.65
0.6~0.8	347	3.11
0.8~1.0	182	1.63
>1.0	169	1.51

性状^a	标记	染色体	物理位置	P值	R²	候选基因	注释	分子功能	备注
T1	PZE-104036105	4	47241320	3.95×10^-5	0.12	Zm00001d049865	CASP-like protein	dehydrogenase	条件分析
T1	SYN16455	4	239628761	1.61×10^-5	0.13	Zm00001d054004	plant-specific domain TIGR01589 family protein	NA	条件分析
T1	SYN38269	9	136583562	8.64×10^-5	0.12	Zm00001d047680	calmodulin-binding protein 60G	DNA-binding transcription factor activity
T2	SYNGENTA5755	1	212194098	2.02×10^-6	0.18	Zm00001d032165	defective in cullin neddylation protein	ubiquitin-like protein conjugating enzyme binding
T2	SYNGENTA5755	1	212194098	2.02×10^-6	0.18	Zm00001d032166	DUF1336 domain- containing protein	defense/immunity protein
T2	PZE-101169962	1	213269897	9.28×10^-6	0.15	Zm00001d032190	MYB family transcription factor	DNA-binding transcription factor
T2	SYN1142	2	9085410	5.07×10^-5	0.12	Zm00001d002275	abc transporter c family member 2-like	ATP-binding cassette (ABC) transporter
T2	SYN1142	2	9085410	5.07×10^-5	0.12	Zm00001d002277	Ubiquitin-like domain- containing protein	ATPase activity; chaperone binding
T2	PHM13742.5	3	215181142	2.77×10^-5	0.13	Zm00001d044090	5ʹ-deoxynucleotidase	phosphatase activity
T2	PHM13742.5	3	215181142	2.77×10^-5	0.13	Zm00001d044091	serine threonine-protein kinase ht1-like	non-receptor serine/threonine protein kinase
T2	PZE-106065133	6	117419198	1.18×10^-6	0.18	Zm00001d037329	uncharacterized protein	NA

统计模型	标记^a	染色体	物理位置	关联性状
一般线性模型	PZE-101167639	1	211083097	株高变化率
	SYNGENTA5755	1	212194098	株高变化率
	PZE-101168916	1	212192906	株高变化率
	PZE-101169962	1	213269897	株高变化率
	PHM13742.5	3	215181142	株高变化率
	PZE-106065133	6	117419198	株高变化率
	SYN4789	6	150688349	鲜重变化率
混合线性模型	SYNGENTA5755	1	212194098	株高变化率
	PZE-101169962	1	213269897	株高变化率
	SYN1142	2	9085410	株高变化率
	PHM13742.5	3	215181142	株高变化率
	PZE-106065133	6	117419198	株高变化率
	PZE-104036105	4	47241320	枯萎度
	SYN16455	4	239628761	枯萎度
	SYN38269	9	136583562	枯萎度

Gene_ID	Primer-F	Primer-R
Zm00001d049865	AATCACCGTCACCTTCAA	GCAGTAGAGGCGGTAGAA
Zm00001d049867	AGGGCTACTTCAACGACC	GCAGCATTCCTCCAGCAC
Zm00001d054004	TATGGGATGCCTGCTATG	CACGGTCTCATTGCCTAA
Zm00001d047680	CTGGAAGCCGTGAGCAAC	CCTTGAACTCGGCTATGC
Zm00001d032165	ATGGGTTCCTGTTTCTCC	TGTTTCAATGCCTTCTGG
Zm00001d032166	TTCAGTTGCCTTACATCC	ACCATCCAATAACCCTCA
Zm00001d050434	CACCTCTTCCGCCAAACA	AGCATCGTCAGAACCTCC
Zm00001d032190	TGCCTGTCCTCCACTTCC	CCAACGTCGGCTTCCTCT
Zm00001d002275	AACCCTTGGCTGTTACGA	AGCCGATGAGAACGAAAG
Zm00001d002277	GCCGAGTACCTGGACGCA	TCTCCCATTTGGTCGTCA
Zm00001d044090	TGGCTCTGATTGCTGGTG	TCCTGCTTTCCGCATCCC
Zm00001d044091	AGTTGTGGTCCAAATAGC	TCTTTACCGTTCTCGTCT
Zm00001d037329	ATGGGCAACAGCATCGGC	GCGTGAGCATGAGCGACT
ACTIN	GCATCCATGAGACCACCTACAAC	GATGGACCCTCCTATCCAGACAC

Genome-wide association study and candidate gene prediction of salt tolerance related traits in maize

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性状^a	SNP1	SNP2	P值	add_R²(%) ^b	epi_R²(%) ^c
T1	NA	NA	NA	25.69	NA
T2	SYNGENTA5755	SYN1142	0.031	34.92	5.24
T2	SYNGENTA5755	PHM13742.5	0.0076	34.92	5.24
T2	SYNGENTA5755	PZE-106065133	0.021	34.92	5.24
T2	SYN1142	PHM13742.5	0.028	34.92	5.24

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