伯克霍尔德菌通过改善生理适应性及调节铝响应基因的表达增强甘蔗对铝胁迫的耐受性

doi:10.17521/cjpe.2024.0014

植物生态学报 ›› 2025, Vol. 49 ›› Issue (3): 475-487.DOI: 10.17521/cjpe.2024.0014 cstr: 32100.14.cjpe.2024.0014

伯克霍尔德菌通过改善生理适应性及调节铝响应基因的表达增强甘蔗对铝胁迫的耐受性

陆珍¹^,², 谢光杰², Qaisar KHAN², 覃英², 黄毓燕², 郭道君², 杨婷婷², 杨丽涛², 邢永秀²^,^*(), 李杨瑞³^,^*(), 王震⁴

¹广西农业科学院园艺研究所, 南宁 530007
²广西大学农学院, 南宁 530004
³广西农业科学院甘蔗研究所/农业农村部广西甘蔗生物技术与遗传改良重点实验室/广西甘蔗遗传改良重点实验室, 南宁 530007
⁴玉林师范学院智慧农业学院, 广西玉林 537000

收稿日期:2024-01-19 接受日期:2024-09-28 出版日期:2025-03-20 发布日期:2025-01-20
通讯作者: * (邢永秀, document126@126.com; 李杨瑞, liyr@gxaas.net)
基金资助:
国家自然科学基金(31471449);国家自然科学基金(31560352);国家现代农业产业技术体系广西甘蔗创新团队项目(gjnytxgxcxtd-2021-03-01);广西创新驱动重大专项(Guike AA22117002-7);中央引导地方科技发展资金项目(Guike ZY23055011);广西自然科学基金(2022GXNSFBA035542)

Burkholderia strains enhance the tolerance of sugarcane to aluminum stress by improving the physiological adaptability and regulating the expression of aluminum responsive genes

LU Zhen¹^,², XIE Guang-Jie², Qaisar KHAN², QIN Ying², HUANG Yu-Yan², GUO Dao-Jun², YANG Ting-Ting², YANG Li-Tao², XING Yong-Xiu²^,^*(), LI Yang-Rui³^,^*(), WANG Zhen⁴

¹Horticultural Research Institute, Guangxi Academy of Agricultural Sciences, Nanning 530007, China
²College of Agriculture, Guangxi University, Nanning 530004, China
³Guangxi Key Laboratory of Sugarcane Genetic Improvement/Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs/Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning 530007, China
⁴Wisdom Agriculture College, Yulin Normal University, Yulin, Guangxi 537000, China

Received:2024-01-19 Accepted:2024-09-28 Online:2025-03-20 Published:2025-01-20
Contact: * (Xing YX, document126@126.com; Li YR, liyr@gxaas.net)
Supported by:
National Natural Science Foundation of China(31471449);National Natural Science Foundation of China(31560352);Guangxi Sugarcane Innovation Team of National Modern Agricultural Industrial Technology System Project(gjnytxgxcxtd-2021-03-01);Guangxi R&D Program Project(Guike AA22117002-7);the Central Government Supported Local R&D Program Project(Guike ZY23055011);Natural Science Foundation of Guangxi(2022GXNSFBA035542)

摘要/Abstract

摘要：

多种因素可影响植物生长并提高其抗逆性, 其中植物根际促生菌(PGPR)可能扮演着极其重要的角色。为挖掘耐铝性良好的根际微生物资源并探讨其缓解甘蔗(Saccharum officinarum)铝毒害的作用, 该研究从甘蔗根际土壤中分离出一批耐铝细菌, 分析它们的促生特性、耐酸性、耐铝性以及对Al³⁺的去除能力, 筛选出优势PGPR并检测其对甘蔗的促生长效应, 对比接种和不接种PGPR的甘蔗在铝胁迫下植株体内的铝积累量、生理代谢情况以及耐铝相关基因的表达量。分离筛选到的3株优势甘蔗根际细菌——伯克霍尔德菌(Burkholderia), A1、A23、X6具有较强的耐酸性(pH 3.8)和耐铝性(4或5 mmol·L^-1), 3株细菌均具有溶磷、分泌胞外多糖(EPS)、固氮和去除Al³⁺的能力, X6能够产生少量吲哚乙酸, A1和X6可分泌较多的铁载体, A23和X6具有1-氨基环丙烷-1-羧酸脱氨酶活性, A1、A23、X6菌株组合可显著提高甘蔗株高、叶面积及地上部分鲜质量。接种组合菌对植株地上部分与地下部分氮、磷、钾的含量无明显影响, 但显著增加了0.5、1 mmol·L^-1铝胁迫下甘蔗地上部分的铝含量和显著降低了1 mmol·L^-1铝胁迫下甘蔗地下部分的铝含量, 总体表现为降低甘蔗体内的总铝含量。接种处理对植株超氧化物歧化酶、过氧化物酶活性以及脯氨酸、可溶性蛋白含量无显著影响, 但显著降低了铝胁迫下甘蔗根尖的丙二醛含量, 显著提高了根尖的过氧化氢酶活性, 显著增加了甘蔗根尖MAPK和GST基因以及叶片PEPC基因的表达量。这些结果表明, 耐铝伯克霍尔德菌对甘蔗生长、铝的吸收积累和植株抗氧化防御能力及耐铝基因表达产生显著影响, 这些影响共同作用提高了甘蔗的耐铝毒能力。

关键词: 伯克霍尔德菌, 甘蔗, 铝胁迫, 生理适应性, 耐铝基因

Abstract:

Aims Many factors can influence the growth of plants and their adaptability to the growing environment, among which plant growth promoting rhizobacteria (PGPR) may play a key role. Thus, the aim of this study is to explore the rhizosphere microbial resources with high aluminum tolerance and investigate their role in alleviating the aluminum toxicity to sugarcane (Saccharum officinarum).
Methods We isolated and screened the dominant strains of aluminum-tolerant PGPR from the rhizosphere soil of sugarcane and studied their effects on sugarcane growth. By measuring the aluminum accumulation, physiological metabolism and expression changes of aluminum-tolerant genes in the aboveground and underground parts of sugarcane under aluminum stress, we compared the aluminum tolerance of sugarcane inoculated with aluminum-tolerant bacteria and those without aluminum-tolerant bacteria.
Important findings Three strains of dominant sugarcane rhizosphere bacteria, Burkholderia A1, A23 and X6, have strong acid tolerance (pH 3.8) and aluminum tolerance (4 or 5 mmol·L^-1). All the three strains have the ability to dissolve phosphorus, secrete exopolysaccharides (EPS), fix nitrogen and remove Al³⁺. X6 can produce low level of indole-3-acetic acid (IAA), A1 and X6 can secrete a certain amount of iron carriers, and A23 and X6 have 1-aminocyclopropane-l-carboxylic acid (ACC) deaminase activity. The combined bacteria of A1, A23 and X6 improved the plant height, leaf area and fresh mass of aboveground part of sugarcane. Although the bacteria combinations showed no obvious effect on the contents of nitrogen, phosphorus and potassium in aboveground and underground parts of plant, but significantly increased the aluminum content in aboveground part of sugarcane under 0.5 and 1 mmol·L^-1 aluminum stress and significantly reduced the aluminum content in underground part of sugarcane under 1 mmol·L^-1 aluminum stress, and the overall performance was reducing the total aluminum content in sugarcane. The inoculation treatment showed no significant effect on the activities of superoxide dismutase (SOD) and peroxidase (POD), and the contents of proline (Pro) and soluble protein (SP), but significantly reduced the malondialdehyde (MDA) content and significantly increased the catalase (CAT) activity in root tips under aluminum stress, and significantly increased the expression of MAPK and GST genes in root tips and PEPC gene in leaves of sugarcane. These results showed that Al-tolerant Burkholderia strains had significant effects on sugarcane growth, aluminum absorption and accumulation, plant antioxidant defense ability and aluminum-tolerant gene expression, which together improved the aluminum tolerance of sugarcane.

Key words: Burkholderia, Saccharum officinarum, aluminum stress, physiological adaptation, aluminum tolerant gene

陆珍, 谢光杰, Qaisar KHAN, 覃英, 黄毓燕, 郭道君, 杨婷婷, 杨丽涛, 邢永秀, 李杨瑞, 王震. 伯克霍尔德菌通过改善生理适应性及调节铝响应基因的表达增强甘蔗对铝胁迫的耐受性. 植物生态学报, 2025, 49(3): 475-487. DOI: 10.17521/cjpe.2024.0014

LU Zhen, XIE Guang-Jie, Qaisar KHAN, QIN Ying, HUANG Yu-Yan, GUO Dao-Jun, YANG Ting-Ting, YANG Li-Tao, XING Yong-Xiu, LI Yang-Rui, WANG Zhen. Burkholderia strains enhance the tolerance of sugarcane to aluminum stress by improving the physiological adaptability and regulating the expression of aluminum responsive genes. Chinese Journal of Plant Ecology, 2025, 49(3): 475-487. DOI: 10.17521/cjpe.2024.0014

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2024.0014

https://www.plant-ecology.com/CN/Y2025/V49/I3/475

图/表 11

表1 甘蔗铝响应相关基因荧光定量PCR引物信息

Table 1 Information of primers for quantitative real-time PCR of aluminum response related genes in sugarcane

基因 Gene	上游引物 Forward primer (5′-3′)	下游引物 Reverse primer (5′-3′)
GAPDH	CACGGCCACTGGAAGCA	TCCTCAGGGTTCCTGATGCC
MAPK	CATCGAGCGGATGCTAACCT	AGTCGAACGAGAATGGCTCC
GST	TACATGGCACACCCTGCATT	AGGAACAATACGACGGAGCA
PEPC	TCCACAGGATGAAATGCGCT	TGTAGGGAAGGCGCTGATTG

表2 甘蔗根际耐铝细菌的促生特性(平均值±标准差)

Table 2 Growth-promoting characteristics of aluminum-tolerant bacteria from the rhizosphere soil of sugarcane (mean ± SD)

菌株 Baterial stain	产IAA能力 Capacity for producing IAA	磷增溶 Phosphorus solubilization (mg·L^-1)	铁载体相对含量 Relative content of siderophore (A/Ar)	固氮 Nitrogen fixation	ACC脱氨酶活性 ACC deaminase activity	胞外多糖 EPS (mg·mL^-1)
A1	-	54.94 ± 2.38^a	0.38 ± 0.03^a	+++	-	0.27 ± 0.03^c
A23	-	59.32 ± 0.99^a	-	+	+	1.29 ± 0.12^b
X6	+	59.42 ± 3.41^a	0.43 ± 0.02^b	+++	+	1.68 ± 0.07^a

图1 基于16S rRNA基因构建的3株甘蔗根际耐铝细菌的系统发育进化树。

Fig. 1 Phylogenetic tree of three strains of aluminum-tolerant bacteria from sugarcane rhizosphere based on 16S rRNA gene.

图2 培养基不同pH对耐铝细菌菌株(A1、A23、X6)生长的影响(平均值±标准差)。不同小写字母表示差异显著(p < 0.05)。OD600, 菌液在600 nm波长处的吸光值。

Fig. 2 Effect of different acidity of culture medium on growth of the aluminum-tolerant bacterial strains (A1, A23, X6) (mean ± SD). Different lowercase letters indicate significant differences (p < 0.05). OD600, the optical density of bacterial suspension at 600 nm.

图3 不同Al3+浓度对耐铝细菌菌株(A1、A23、X6)生长的影响(平均值±标准差)。同一铝浓度处理下, 左边的数据表示OD600值, 右边的数据表示最终pH。OD600为菌液在600 nm波长处的吸光值, 不同小写字母表示差异显著(p < 0.05)。

Fig. 3 Effects of different Al3+ concentrations on the growth of aluminum-tolerant bacterial strains (A1, A23, X6) (mean ± SD). Under the same aluminum concentration treatment, the data on the left represent the OD600 values, and those on the right represent the final pH values. OD600 is the optical density of bacterial suspension at 600 nm, different lowercase letters indicate significant differences (p < 0.05).

表3 甘蔗根际耐铝细菌生长2天后培养液剩余Al3+含量及pH的变化(平均值±标准差)

Table 3 Changes of residual Al3+ content and pH of culture solution after aluminum-tolerant bacteria from the rhizosphere soil of sugarcane growth 2 days (mean ± SD)

菌株 Bacterial strain	最终pH Final pH	上清液中的Al³⁺浓度 Al³⁺ concentration in supernatant (mmol·L^-1)	剩余Al³⁺百分比 Percentage of residual Al³⁺ (%)
CK	4.50 ± 0.00^c	0.995 ± 0.003^a	99.539 ± 0.003^a
A1	7.91 ± 0.16^a	0.816 ± 0.042^b	81.992 ± 4.038^b
A23	7.02 ± 0.04^b	0.825 ± 0.014^b	82.880 ± 1.331^b
X6	7.79 ± 0.20^a	0.772 ± 0.007^b	77.581 ± 0.830^b

表4 混合耐铝细菌接种(T)对甘蔗农艺性状的影响(平均值±标准差)

Table 4 Effects of aluminum-tolerant bacterial strain mixture inoculation (T) on agronomic traits of sugarcane (mean ± SD)

处理 Treatment	株高 Plant height (cm)	叶面积 Leaf area (cm²)	干质量 Dry mass (g)		鲜质量 Fresh mass (g)
处理 Treatment	株高 Plant height (cm)	叶面积 Leaf area (cm²)	地上部分 Aboveground part	地下部分 Underground part	地上部分 Aboveground part	地下部分 Underground part
CK	23.53 ± 1.72^b	12.84 ± 1.37^b	5.96 ± 1.14^a	1.06 ± 0.15^a	26.25 ± 6.73^b	8.00 ± 2.83^a
T	29.40 ± 0.47^a	18.14 ± 2.57^a	8.49 ± 1.13^a	1.20 ± 0.09^a	36.80 ± 7.78^a	10.90 ± 0.42^a

图4 苏木精染色的甘蔗根尖。T, 混合耐铝细菌接种。

Fig. 4 Hematoxylin stained sugarcane root tips. T, aluminum- tolerant bacterial strain mixture inoculation.

图5 接种耐铝细菌(T)对铝胁迫下甘蔗地上部分与地下部分全氮含量(A)、全磷含量(B)、全钾含量(C)以及全铝含量(D)的影响(平均值±标准差)。各部分不同小写字母表示不同浓度和处理间差异显著(p < 0.05)。

Fig. 5 Effects of aluminum-tolerant bacteria inoculation (T) on total nitrogen (A), total phosphorus (B), total potassium (C) and total aluminum (D) contents in shoot and root of sugarcane under aluminum stress (mean ± SD). Different lowercase letters in the same part indicate significant differences among different concentrations and treatments (p < 0.05).

图6 接种耐铝细菌(T)对铝胁迫下甘蔗叶片和根尖中超氧化物歧化酶(SOD) (A)、过氧化氢酶(CAT) (B)、过氧化物酶(POD) (C)活性及可溶性蛋白(SP) (D)、脯氨酸(Pro) (E)、丙二醛(MDA) (F)含量的影响(平均值±标准差)。同一器官不同小写字母表示不同浓度和处理间差异显著(p < 0.05)。

Fig. 6 Effects of aluminum-tolerant bacteria inoculation (T) on superoxide dismutase (SOD) (A), catalase (CAT) (B) and peroxidase (POD) (C) activities and soluble protein (SP) (D), proline (Pro) (E) and malondialdehyde (MDA) (F) contents in sugarcane leaves and root tips under aluminum stress (mean ± SD). Different lowercase letters in the same organ indicate significant differences among different concentrations and treatments (p < 0.05).

图7 铝胁迫下甘蔗根尖和叶片耐铝相关基因MAPK (A)、GST (B)和PEPC (C)表达量的变化(平均值±标准差)。同一部分不同小写字母表示不同浓度和处理间差异显著(p < 0.05)。T, 混合耐铝细菌接种。

Fig. 7 Changes in the expression of aluminum tolerance related genes MAPK (A), GST (B) and PEPC (C) in sugarcane root tips and leaves under aluminum stress (mean ± SD). Different lowercase letters in the same part indicate significant differences among different concentrations and treatments in leaves and roots at the level p < 0.05. T, aluminum-tolerant bacterial strain mixture inoculation.

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伯克霍尔德菌通过改善生理适应性及调节铝响应基因的表达增强甘蔗对铝胁迫的耐受性

Burkholderia strains enhance the tolerance of sugarcane to aluminum stress by improving the physiological adaptability and regulating the expression of aluminum responsive genes

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