玉米自然群体苗期耐盐性鉴定及耐盐相关基因分析

doi:10.3864/j.issn.0578-1752.2025.20.005

Abstract

Abstract:

【Objective】Soil salinization significantly impairs the growth and development of maize, resulting in reduced yields. Investigating the salt tolerance of various maize inbred lines and identifying favorable allelic variants associated with salt tolerance can provide valuable SNP markers and candidate gene resources for salt-tolerant maize varieties.【Method】This study utilized a natural population comprising 238 inbred maize lines as experimental materials. Twenty-day-old maize seedlings at the three-leaf stage were subjected to treatment with a 300 mmol·L^-1 NaCl solution, and changes in biomass, moisture contents as well as salt damage phenotypes were evaluated after 40 days of salt stress. A genome-wide association study (GWAS) was subsequently performed to identify favorable allelic variants associated with salt tolerance in maize.【Result】Through salt tolerance assessment of a maize natural population at the seedling stage, the materials were categorized into five distinct salt tolerance grades based on the salt damage rate: 22 highly tolerant materials (Grade 1), 93 tolerant materials (Grade 2), 62 moderately tolerant materials (Grade 3), 41 salt-sensitive materials (Grade 4), and 20 highly sensitive materials (Grade 5). The number of materials with different salt tolerance levels shows a normal distribution characteristic, with high-tolerance and highly sensitive materials comprising 17.6% of the total, while intermediate-grade materials accounted for 82.4%. Statistical analysis revealed that the salt damage rate was significantly and negatively correlated with the fresh weight, dry weight, and moisture content of plants under salt stress. The investigated traits exhibited considerable variability, indicating substantial differences among the genotypes. Genome-wide association analysis identified a total of 40 SNP loci associated with maize salt tolerance. Further investigation revealed one significantly associated SNP locus on chromosome 1 and another on chromosome 10. Analysis of the candidate genes within the 100 Kb confidence interval upstream and downstream of these two loci identified a total of 18 functional genes, including 9 genes with functional annotations and 9 genes with unknown functions.【Conclusion】22 first-class salt-tolerant maize inbred line materials were selected from a natural population consisting of 238 lines. 40 SNP loci associated with salt tolerance in maize seedlings were identified, among which two key SNPs showed significant association with the trait. Two salt tolerance-related candidate genes, ZmSTYK46 and Zm00001eb004810, were identified. ZmSTYK46 encodes a serine/threonine protein kinase, while the function of Zm00001eb004810 remains unknown.

Key words: Zea mays L., inbred lines, salt tolerance identification, genome-wide association analysis, salt tolerance functional genes

WU ShuYu, HENG YanFang, YU TaiFei, WANG ShiJia, YU SiJia, LI Yuan, HU Zheng, ZHANG Hui, SUN XianJun, LI Liang, JIANG QiYan. Identification of Salt Tolerance in Maize Natural Populations at the Seedling Stage and Analysis of Salt Tolerance-Associated Genes[J].Scientia Agricultura Sinica, 2025, 58(20): 4085-4099.

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Figures/Tables 12

Table 1

Criteria for determining salt damage rate based on plant phenotype under salt stress"

盐害率 SDR (%)	植株表型 Plant phenotype
<10	生长正常或基本正常，无受害症状或叶尖干枯 Growth is within the normal range or essentially normal, with no observed symptoms of damage or dry leaf tips
10-20	第一片叶有半片及以下干枯，其余部分正常生长 The first leaf exhibits partial withering, with half or less of its surface affected, while the remainder continues to develop normally
20-30	第一片叶半片以上干枯或全部干枯，其余部分正常生长 The first leaf is more than half dried or fully desiccated, whereas the remainder of the plant continues to develop normally
30-40	第一片叶全部干枯，第二片叶半片及以下干枯，其余部分正常生长 The first leaf is entirely withered, the second leaf exhibits withering that affects half or less of its surface, and the remaining leaves are growing normally
40-50	第一片叶全部干枯，第二片叶半片以上干枯或全部干枯，其余部分正常生长 The first leaf is entirely withered, and more than half of the second leaf is either withered or fully withered as well, while the remainder of the plant exhibits normal growth
50-60	前两片叶全部干枯，叶心部分发黄未超过1/2，未干枯 The first two leaves are entirely withered, and the yellowing of the leaf center does not extend beyond one-half and remains non-withered
60-70	前两片叶全部干枯，叶心部分发黄超过1/2，未干枯 The first two leaves are entirely withered, and over half of the central portion of the leaf has turned yellow and remains non-withered
70-80	叶片基本全部干枯，茎部正常生长 The leaves are almost entirely withered, while the stems continue to grow normally
80-90	茎部受害未完全干枯 The stem is partially damaged, although it has not completely dried up
90-100	基本完全干枯 The plant has completely dried up

Table 1

Table 2

Fig. 1

Table 3

Basic information of materials classified as grade 1 highly salt-tolerant and grade 5 highly salt-sensitive"

自交系 Inbred lines	鲜重 Fresh weight (g)	干重 Dry weight (g)	水分含量 Moisture Content (%)	盐害率 Salt damage rate (%)	耐盐等级 Salt tolerance grade	耐盐性 Salt tolerance	类群 Group	耐盐等位变异* Salt-tolerant allelic variation
Chang7_2	6.37±1.03	0.63±0.13	90.12±1.40	1.67±0.67	1	HST	TSPT	11100
Oh43	3.25±0.57	0.30±0.02	90.87±1.81	6.67±0.27	1	HST	Lvda	11100
A3046	2.91±0.54	0.31±0.09	89.47±1.42	6.67±0.67	1	HST	Iodent	-
21N35755	7.92±0.77	0.91±0.12	88.50±0.62	11.67±1.33	1	HST	BSSS	-
M-LD656	6.11±0.96	0.61±0.11	90.00±1.39	12.00±1.69	1	HST	Lancaster	11110
LH191	6.67±0.90	0.82±0.09	87.65±1.42	13.33±1.26	1	HST	-	-
PHP76	5.10±0.79	0.50±0.09	90.12±1.29	13.33±1.33	1	HST	Iodent	-
PHG35	5.72±0.76	0.58±0.07	89.87±0.34	13.33±0.33	1	HST	BSSS	11100
M-DH969-ZW	3.37±0.91	0.36±0.06	89.44±1.52	14.00±1.66	1	HST	BSSS	01100
2004005029	3.67±0.20	0.45±0.04	87.77±0.52	15.00±1.00	1	HST	Flint	10100
LH163	7.93±1.08	0.84±0.18	89.44±0.55	16.67±1.28	1	HST	Iodent	-
WIL_18	7.86±0.69	0.82±0.06	89.60±0.22	16.67±0.67	1	HST	TSPT	01100
PHBA6	4.21±0.69	0.46±0.04	89.06±1.91	17.67±1.88	1	HST	Lancaster	11100
W22	6.38±0.44	0.67±0.04	89.44±0.80	18.33±2.93	1	HST	Lancaster	11100
Lx9801	7.43±1.01	0.83±0.20	88.88±0.88	18.33±1.41	1	HST	TSPT	11100
丹3130 Dan3130	4.40±0.33	0.46±0.05	89.54±0.49	18.33±1.26	1	HST	Lancaster	11100
WPH-PB21-303	6.17±1.04	0.70±0.11	88.65±1.27	18.33±1.33	1	HST	Flint	-
2004011031	8.20±0.26	0.99±0.07	87.91±1.12	19.00±1.54	1	HST	Iodent	10100
200B	7.81±1.10	0.89±0.12	88.59±1.08	19.33±1.35	1	HST	Flint	11100
21N35798	5.16±0.83	0.55±0.08	89.34±0.54	20.00±1.56	1	HST	Reid	11111
PHN82	3.32±0.29	0.46±0.01	86.19±1.11	20.00±1.00	1	HST	Iodent	11100
PHR58	4.93±0.41	0.49±0.05	90.12±0.52	20.00±1.66	1	HST	P78599	11100
6F629	2.18±0.32	0.38±0.01	82.44±2.06	81.67±1.33	5	HSS	BSSS	-
Dahuang46	1.10±0.48	0.19±0.07	82.39±5.35	81.67±1.01	5	HSS	TSPT	11100
LIBC_4	1.47±0.35	0.31±0.05	78.97±2.9	81.67±1.67	5	HSS	Iodent	-
F-JY201	2.13±0.29	0.43±0.08	79.56±1.49	83.33±1.33	5	HSS	Lancaster	11100
21N35812	1.94±0.04	0.42±0.04	78.45±1.64	83.33±1.26	5	HSS	BSSS	10100
PHN66	2.01±0.21	0.47±0.02	76.79±2.04	83.33±1.41	5	HSS	BSSS	-
PHRKB	1.46±0.29	0.39±0.06	73.68±1.78	83.33±1.26	5	HSS	BSSS	10000
PHR55	1.46±0.39	0.31±0.09	78.59±0.77	85.00±1.64	5	HSS	Iodent	-
LH192	1.61±0.26	0.29±0.06	82.13±1.30	85.00±1.77	5	HSS	BSSS	10100
2004010028	2.50±0.46	0.45±0.04	82.05±0.54	85.00±1.00	5	HSS	BSSS	00100
21N35716	1.85±0.45	0.49±0.06	73.33±0.81	88.33±1.41	5	HSS	Flint	10100
丹6263 Dan6263	1.26±0.27	0.31±0.04	75.66±0.34	90.00±1.89	5	HSS	Reid	11100
Baihunhuang	1.11±0.60	0.25±0.08	77.83±0.25	90.00±1.77	5	HSS	其他类型 Other	11000
WIL_3	1.72±0.27	0.43±0.05	74.98±0.13	91.67±1.41	5	HSS	Iodent	11000
LH195	0.68±0.26	0.15±0.10	77.53±0.67	91.67±2.01	5	HSS	其他类型 Other	10100
21N35655	1.62±0.11	0.56±0.12	65.75±1.02	93.33±0.67	5	HSS	Reid	11100
Shuang741	2.55±0.16	0.33±0.09	87.26±1.99	93.33±0.67	5	HSS	TSPT	11110
21N35915	0.98±0.35	0.26±0.03	73.08±1.43	93.33±1.41	5	HSS	P78599	01100
21N35658	0.66±0.17	0.21±0.02	68.35±0.07	96.67±0.67	5	HSS	Reid	-
M-LY99	0.46±0.09	0.21±0.02	53.74±0.77	100.00±0.00	5	HSS	Iodent	-

Table 3

Table 4

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Fig. 6

Table 5

Candidate gene analysis of SNP locus confidence intervals"

染色体 Chr.	候选基因 Candidate genes	基因注释 Gene annotation	基因功能 Gene function	基因功能结构域 Gene functional domain
Chr.1	Zm00001eb004800	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.1	Zm00001eb004810	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.1	Zm00001eb004820	组蛋白H2A变异体1 Histone H2A variant 1 (H2HA1)	DNA结合蛋白异二聚体化活性DNA binding protein heterodimerization activity	C端组蛋白H2A C-terminus histone H2A
Chr.1	Zm00001eb004830	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.1	Zm00001eb004840	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.1	Zm00001eb004850	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.1	Zm00001eb004860	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.10	Zm00001eb434270	3-异丙基苹果酸脱氢酶2 3-isopropylmalate dehydrogenase 2 (IPMDH2)	异柠檬酸/异丙基苹果酸脱氢酶，保守位点 Isocitrate/isopropylmalate dehydrogenase, conserved site	异柠檬酸/异丙基苹果酸脱氢酶 Isocitrate/isopropylmalate dehydrogenase
Chr.10	Zm00001eb434280	丝氨酸/苏氨酸蛋白激酶ATG1t（ATG1t）Serine/threonine-protein kinase ATG1t (ATG1t)	丝氨酸/苏氨酸蛋白激酶ATG1t，膜的整合组成部分，ATP结合（结构/区域） Serine/threonine-protein kinase ATG1t integral component of membrane ATP binding	蛋白激酶结构域 Protein kinase domain
Chr.10	Zm00001eb434290	丝氨酸/苏氨酸蛋白激酶STY46（STYK46）Serine/threonine-protein kinase STY46 (STYK46)	非特异性丝氨酸/苏氨酸蛋白激酶，ATP结合（结构/区域） Non-specific serine/threonine protein kinase ATP binding	蛋白激酶结构域 Protein kinase domain
Chr.10	Zm00001eb434300	SKP1相互作用蛋白15（SKIP15） SKP1-interacting partner 15 (SKIP15)	SKP1相互作用蛋白15，蛋白质结合（结构/区域） SKP1-interacting partner 15 binding	_
Chr.10	Zm00001eb434310	液泡铁转运蛋白5（VIT5） Vacuolar iron transporter 5 (VIT5)	液泡铁转运蛋白，铁/锰离子跨膜转运活性 Vacuolar iron transporter iron/manganese ion transmembrane transporter activity	液泡铁转运蛋白家族 VIT family
Chr.10	Zm00001eb434320	可溶性无机焦磷酸酶（PPases） Soluble inorganic pyrophosphatase (PPases)	可溶性无机焦磷酸酶，镁离子结合（结构/区域），无机二磷酸酶活性 Soluble inorganic pyrophosphatase magnesium ion binding inorganic diphosphatase activity	无机焦磷酸酶 Inorganic pyrophosphatase
Chr.10	Zm00001eb434330	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.10	Zm00001eb434350	过氧化物酶12前体（POD12）Peroxidase 12 precursor (POD12)	过氧化物酶血红素结合（结构/区域），金属离子结合（结构/区域） Peroxidase heme binding metal ion binding	过氧化物酶 Peroxidase
Chr.10	Zm00001eb434360	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.10	Zm00001eb434370	未知蛋白 Uncharacterized protein	未知功能 Uncharacterized function	_
Chr.10	Zm00001eb434380	生长素响应因子13（ARF13） Auxin response factor 13 (ARF13)	DNA 结合（型）生长素响应因子 DNA binding Auxin response factor	植物特异性B3-DNA 结合结构域 Plant-specific B3-DNA binding domain

Table 5

Fig. 7

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盐害率 SDR (%)	耐盐等级 Salt tolerance grade	耐盐性 Salt tolerance
0≤SDR≤20	1级 Grade 1	高耐 High salt tolerance
20<SDR≤40	2级 Grade 2	耐盐 Salt tolerance
40<SDR≤60	3级 Grade 3	中耐 Moderately salt tolerance
60<SDR≤80	4级 Grade 4	敏感 Salt sensitivity
80<SDR≤100	5级 Grade 5	高敏 High salt sensitivity

指标 Index	平均值 Average value	标准差 Standard deviation	变异系数 Coefficient of variation (%)
盐胁迫条件下鲜重 Fresh weight under salt stress (g)	3.53	1.62	45.89
盐胁迫条件下干重 Dry weight under salt stress (g)	0.46	0.16	34.78
盐胁迫条件下水分含量 Moisture content under salt stress (%)	85.61	4.63	5.41
盐害率 Salt damage rate (%)	46.14	21.69	47.01

Identification of Salt Tolerance in Maize Natural Populations at the Seedling Stage and Analysis of Salt Tolerance-Associated Genes

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