施氮水平影响蚯蚓介导的番茄生长及抗虫性

doi:10.17520/biods.2018245

生物多样性 ›› 2018, Vol. 26 ›› Issue (12): 1296-1307. DOI: 10.17520/biods.2018245

所属专题：土壤生物与土壤健康

• 研究报告: 动物多样性 • 上一篇下一篇

施氮水平影响蚯蚓介导的番茄生长及抗虫性

张宇¹, 肖正高¹, 蒋林惠¹, 钱蕾², 陈小云¹, 陈法军², 胡锋¹, 刘满强^1,^*()

1 南京农业大学资源与环境科学学院土壤生态实验室, 南京 210095
2 南京农业大学植物保护学院, 南京 210095

收稿日期:2018-09-12 接受日期:2018-11-19 出版日期:2018-12-20 发布日期:2019-02-11
通讯作者: 刘满强
作者简介:# 共同第一作者
基金资助:
国家重点研发计划(2016YFD0200305)、国家自然科学基金(41771287)、公益性行业(农业)科研专项(201503121)和江苏高校优势学科(PAPD)

Nitrogen levels modify earthworm-mediated tomato growth and resistance to pests

Yu Zhang¹, Zhenggao Xiao¹, Linhui Jiang¹, Lei Qian², Xiaoyun Chen¹, Fajun Chen², Feng Hu¹, Manqiang Liu^1,^*()

1 Soil Ecology Laboratory, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095
2 College of Plant Protection, Nanjing Agricultural University, Nanjing 210095

Received:2018-09-12 Accepted:2018-11-19 Online:2018-12-20 Published:2019-02-11
Contact: Liu Manqiang
About author:# 同等贡献作者 Contributed equally to this work

摘要/Abstract

摘要：

过量施用氮肥不仅导致严重的生态环境问题, 还会限制土壤生物驱动的生态系统服务功能。蚯蚓的取食和掘穴等活动可以促进土壤肥力和植物生长, 进而影响植物与病虫害的关系。了解氮肥与害虫作用下蚯蚓对植物抗虫性的影响, 有助于揭示土壤动物的生态功能调控机制。采用蚯蚓(威廉腔环蚓Metaphire guillelmi)、西花蓟马(Frankliniella occidentalis)和氮肥用量的三因子完全交互设计, 利用番茄(Lycopersicon esculentum)盆栽实验探索了不同氮水平下蚯蚓对番茄生长及对植食者抗性的影响。结果表明, 在低氮条件下蚯蚓显著降低了番茄茎叶干生物量、根系干生物量及茎叶可溶性糖含量, 而茎叶的茉莉酸和水杨酸含量分别是无蚯蚓对照的6倍和3倍, 且伴随着西花蓟马数量下降了58%。在高氮水平时, 蚯蚓未影响番茄茎叶茉莉酸、茎叶水杨酸含量及西花蓟马数量。蚯蚓介导的番茄营养物质(茎叶可溶性糖和茎叶全氮)和防御信号物质(茎叶茉莉酸和茎叶水杨酸)含量分别与西花蓟马数量呈显著的正相关和负相关。总之, 氮肥施用改变的土壤氮有效性通过改变植物资源和防御物质含量转变了蚯蚓介导的植物抗虫性响应; 全面了解土壤生物对植物生长的影响需要综合考虑土壤管理-土壤动物-植物病原物三者之间的关系。

关键词: 土壤动物, 植物化学组成, 害虫, 地上和地下部, 生态系统服务

Abstract

Excessive chemical nitrogen (N) fertilizer application causes serious environmental problems and affects the ecosystem services that depend on soil biota. Earthworms improve soil fertility and plant productivity via activities such as feeding, burrowing and casting, and alter the relationships between crop plants and pests by modifying plant primary and secondary productivity. In order to mechanistically understand the functional roles of soil fauna in ecosystem services, a pot experiment using tomatoes (Lycopersicon esculentum) was conducted in a greenhouse. The study used a complete factorial design that manipulated earthworm (Metaphire guillelmi) abundance, western flower thrips (Frankliniella occidentalis) and N input. Results showed that under low N-input conditions, earthworms significantly reduced shoot and root biomass and shoot soluble sugar content, and increased shoot jasmonic acid content (by 6 times) and shoot salicylic acid content (by 3 times), compared to treatments without earthworms. This was accompanied by the decrease of thrips abundance by 58%, indicating a remarkable suppression of aboveground pests by earthworms. However, under high N-input conditions, earthworm presence did not affect the contents of shoot jasmonic acid or shoot salicylic acid or thrips abundance by the end of the experimental period (45 days). The earthworm-mediated responses of plant nutrition (shoot soluble sugar and shoot total nitrogen) was significantly positively correlated with thrips abundance, whereas defense (shoot jasmonic and salicylic acid) was significantly negatively correlated. Changes to soil N availability due to N fertilizer input can shift the direction of earthworm-mediated plant resistance against herbivores by altering plant resource acquisition and secondary defense. Effects of earthworms on plant growth and resistance depend on soil management practices such as N fertilizer application. A comprehensive understanding of the roles of soil biota in mediating plant growth requires knowledge of the multifaceted relationships among soil management, soil fauna, and plant pathogens.

Key words: soil fauna, plant chemistry, pests, aboveground-belowground, ecosystem service

张宇, 肖正高, 蒋林惠, 钱蕾, 陈小云, 陈法军, 胡锋, 刘满强 (2018) 施氮水平影响蚯蚓介导的番茄生长及抗虫性. 生物多样性, 26, 1296-1307. DOI: 10.17520/biods.2018245.

Yu Zhang, Zhenggao Xiao, Linhui Jiang, Lei Qian, Xiaoyun Chen, Fajun Chen, Feng Hu, Manqiang Liu (2018) Nitrogen levels modify earthworm-mediated tomato growth and resistance to pests. Biodiversity Science, 26, 1296-1307. DOI: 10.17520/biods.2018245.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2018245

https://www.biodiversity-science.net/CN/Y2018/V26/I12/1296

图/表 8

表1 不同处理下威廉腔环蚓的数量及生物量变化

Table 1 Changes in biomass and number of Metaphire guillelmi under different treatments

处理 Treatments		接种时 Inoculation time		采样时 Sampling time		蚯蚓失重率 Weight loss of the earthworm (%)
处理 Treatments		数量 Number	生物量 Biomass (g)	数量 Number	生物量 Biomass (g)	蚯蚓失重率 Weight loss of the earthworm (%)
无西花蓟马 -WFT	低氮 Low N 高氮 High N	3	10.49 ± 0.27	3	9.19 ± 0.34	12.39
无西花蓟马 -WFT	低氮 Low N 高氮 High N	3	10.35 ± 0.24	3	8.63 ± 0.47	16.62
接种西花蓟马 +WFT	低氮 Low N 高氮 High N	3	10.19 ± 0.19	3	8.52 ± 0.22	16.39
接种西花蓟马 +WFT	低氮 Low N 高氮 High N	3	10.27 ± 0.26	3	7.85 ± 0.66	23.56

表2 蚯蚓、氮素及植食者因素对土壤硝态氮、铵态氮、微生物生物量碳含量和微生物生物量氮含量影响的方差分析结果

Table 2 ANOVA results showing the effects of earthworm, nitrogen and herbivore on the contents of NO3--N, NH4+-N, microbial biomass carbon and microbial biomass nitrogen in soils

变量 Variables	蚯蚓 Earthworm (E) (df = 1)	氮素 Nitrogen (N) (df = 1)	西花蓟马 Thrips (WFT) (df = 1)	E × N (df = 1)	E × WFT (df = 1)	N × WFT (df = 1)	E × N × WFT (df = 1)
硝态氮 NO₃^--N	18.49^***	87.43^***	8.21^**	18.02^***	3.51	6.67*	3.68
铵态氮 NH₄⁺-N	4.07	2.06	10.82^**	1.91	27.26^***	0.00	0.28
微生物生物量碳 Microbial biomass carbon	10.35^**	1.00	60.26^***	2.66	0.99	15.51^***	2.00
微生物生物量氮 Microbial biomass nitrogen	11.94^**	0.38	2.69	0.84	3.90	2.44	23.70^***

图1 不同氮素条件下, 蚯蚓在西花蓟马(WFT)有无时对土壤硝态氮、铵态氮、微生物生物量碳和微生物生物量氮含量(平均值 ± 标准差, n = 6)的影响。-WFT和+WFT分别表示无西花蓟马和有西花蓟马。不同小写字母表示各处理间差异显著(Fisher’s LSD检验, P < 0.05)。

Fig. 1 Effects of earthworm Metaphire guillelmi on the contents of soil NO3 --N, NH4+-N, microbial biomass carbon and microbial biomass nitrogen in the absence or presence of western flower thrips (WFT) under low and high N inputs (mean ± SD, n = 6). In the figure, -WFT and +WFT indicate without and with western flower thrips, respectively. Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors.

表3 蚯蚓、氮素、植食者因素及其交互作用对番茄茎叶及根系营养和化学防御性状的影响

Table 3 Effects of earthworm, nitrogen, herbivore and their interactions on the nutrients and chemical traits of tomato shoots and roots

变量 Variables	蚯蚓 Earthworm (E) (df = 1)	氮素 Nitrogen (N) (df = 1)	西花蓟马 Thrips (WFT) (df = 1)	E × N (df = 1)	E × WFT (df = 1)	N × WFT (df = 1)	E × N × WFT (df = 1)
茎叶干生物量 Shoot dry biomass	22.49^***	117.88^***	10.36^**	2.39	1.64	5.86^*	0.05
根系干生物量 Root dry biomass	13.77^***	2.08	0.20	11.47^**	0.00	0.22	1.68
茎叶可溶性糖 Shoot soluble sugar	25.21^***	2.09	15.47^***	17.79^***	2.01	0.03	0.03
根系可溶性糖 Root soluble sugar	0.01	0.71	2.68	2.17	3.69	1.39	13.09^***
茎叶全氮 Shoot total nitrogen	12.21^**	182.83^***	1.19	3.10	0.00	0.07	1.70
根系全氮 Root total nitrogen	20.37^***	246.77^***	15.21^***	0.06	11.12^**	2.79	2.11
茎叶游离氨基酸 Shoot amino acid	0.97	20.43^***	7.57^**	0.73	0.28	26.10^***	8.31^**
根系游离氨基酸 Root amino acid	46.10^***	43.08^***	7.38^**	21.88^***	14.80^***	32.87^***	0.96
茎叶酚 Shoot phenolics	2.36	36.23^***	4.75^*	1.50	2.26	0.31	29.01^***
根系酚 Root phenolics	3.61	0.01	51.47^***	9.75^**	0.00	0.01	33.56^***
茎叶水杨酸 Shoot salicylic acid	49.52^***	0.08	0.11	72.61^***	80.09^***	18.73^***	95.11^***
茎叶茉莉酸 Shoot jasmonic acid	156.85^***	3.54	26.94^***	38.62^***	83.52^***	64.95^***	116.73^***

图2 不同氮素条件下, 蚯蚓在西花蓟马(WFT)有无时对番茄茎叶干生物量、根系干生物量、茎叶可溶性糖、根系可溶性糖、茎叶游离氨基酸、根系游离氨基酸、茎叶全氮和根系全氮(平均值 ± 标准差, n = 6)的影响。-WFT和+WFT分别表示无西花蓟马和接种西花蓟马。不同小写字母表示各处理间差异显著(Fisher’s LSD检验, P < 0.05)。

Fig. 2 Effects of earthworm Metaphire guillelmi on the contents of tomato shoot dry biomass, root dry biomass, shoot soluble sugar, root soluble sugar, shoot amino acid, root amino acid, shoot total nitrogen and root total nitrogen in the absence or presence of western flower thrips under low and high N inputs (mean ± SD, n = 6). In the figure, -WFT and +WFT indicate without and with western flower thrips, respectively. Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors.

图3 不同氮素条件下, 蚯蚓在西花蓟马(WFT)有无时对番茄茎叶酚、根系酚、茎叶水杨酸和茎叶茉莉酸(平均值 ± 标准差, n = 6)的影响。-WFT和+WFT分别表示无西花蓟马和接种西花蓟马。不同小写字母表示各处理间差异显著(Fisher’s LSD检验, P < 0.05)。

Fig. 3 Effects of earthworm Metaphire guillelmi on the contents of tomato shoot phenolics, root phenolics, shoot jasmonic acid and shoot salicylic acid in the absence or presence of western flower thrips (WFT) under low and high N inputs (mean ± SD, n = 6). In the figure, -WFT and +WFT indicate without and with western flower thrips, respectively. Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors.

图4 蚯蚓和氮素水平对植食者西花蓟马(WFT)种群数量(平均值 ± 标准差, n = 6)的影响。不同小写字母表示各处理间差异显著(Fisher’s LSD检验, P < 0.05)。

Fig. 4 Effects of earthworm and nitrogen level on the abundance of western flower thrips (WFT) (mean ± SD, n = 6). Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors.

图5 蚯蚓介导的番茄营养物质(茎叶可溶性糖和茎叶全氮)及信号物质(茎叶茉莉酸和茎叶水杨酸)与西花蓟马数量(WFT)的关系

Fig. 5 Regressions between western flower thrips (WFT) abundance and contents of tomato shoot soluble sugar, shoot total nitrogen, shoot salicylic acid and shoot jasmonic acid.

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施氮水平影响蚯蚓介导的番茄生长及抗虫性

Nitrogen levels modify earthworm-mediated tomato growth and resistance to pests

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