Interspecific below-ground interactions driven by root exudates in agroecosystems with diverse crops
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摘要: 根系分泌物介导植物种间的地下部相互作用在生物多样性-生态系统功能关系中发挥着重要作用。本文综述了在作物多样性种植体系中, 根系分泌物介导的种间相互作用及其机制。具体包括: 作物的根系分泌物能够活化土壤难溶性养分, 有利于自身和相邻植物的养分吸收; 粮食作物与超累积植物间作, 根系分泌物中有机酸含量改变, 促进超富集作物对重金属的吸收, 降低粮食作物对重金属的吸收; 作物多样性通过改变根系分泌物的种类和组成, 调控微生物群落结构, 减少病原菌; 信号物质介导的物种间相互识别作用, 引起相邻植物一系列的表型可塑性和生理响应, 比如化感物质会抑制相邻植物, 抑制杂草的萌芽和生长。与此同时, 新方法的引入和学科间的交叉, 为未来根系分泌物在作物多样性体系中的研究和应用提供了新的手段、角度和方向。这些进展有助于通过利用不同物种根分泌物和信号物质, 实现种间促进作用来提高资源利用率, 降低病虫和杂草发生危害, 减少化肥农药的投入, 为构建可持续的农业生态系统提供理论依据。Abstract: Interspecific interactions mediated by root exudates play an important role in biodiversity-ecosystem functioning (BEF) relationships. We reviewed and explained the advances in interspecific root-root interactions mediated by root exudates in agroecosystems with crop diversification, and highlighted the following: root exudates mobilize insoluble nutrients in the soil, facilitating the uptake of nutrients by the crop and neighboring plants; the increased accumulation of heavy metals by hyperaccumulating plants can reduce the accumulation of heavy metals in associated food crops; alteration of soil microbial community mediated by root exudates from one species can reduce the pathogens in the other crop species; root exudates, as signal substances, also play important roles in mediating the root-root recognition and plasticity response between species; for example, field weeds can be suppressed by root exudates from intercropped allelopathy plants with field crops. In addition, we highlighted some perspectives on practical applications and new methods of research on root exudates in crop diversification systems. These advances provide a theoretical basis for building sustainable agricultural ecosystems by matching the root secretions and signaling substances of different crop species, improving resource utilization, reducing pests and diseases through enhanced interspecific facilitation, and reducing fertilizer and pesticide inputs owing to suppression of weeds through allelopathic effects.
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图 1 根系分泌物介导的种间相互作用
Figure 1. Interspecific interactions mediated by root exudates
根系分泌物可以活化养分促进相邻作物的吸收, 促进豆科(Leguminosae)作物结瘤固氮; 根系分泌物可以调控微生物群落, 减少病害的发生; 根系分泌物中的信号物质介导根系间的相互识别作用, 从而引起响应机制; 根系分泌物中的化感物质抑制相邻植物的生长。Root exudates mobilize sparingly soluble nutrients in the soil, facilitating the uptake of nutrients by the plant itself and neighboring plants, improving the nodulation of legumes. The alteration of soil microbial community mediated by root exudates from one species can control the disease of the other crop species. Root exudates, as signal substances, also play some roles in mediating the root-root recognition between species, neighboring plants can be suppressed by root exudates from intercropped allelopathy plants.
图 2 玉米/蚕豆间作体系中氮高效利用机制
Figure 2. Mechanisms of efficient N utilization at maize/faba bean intercropping system
a: 玉米竞争土壤中氮素缓解氮阻遏现象, 促进蚕豆结瘤固氮; b: 玉米根系分泌物中的黄酮类化合物促进蚕豆染料木素的合成, 并通过增强基因水平和生理水平固氮相关蛋白的活性刺激固氮; 玉米根系分泌物促进了蚕豆固氮基因CFI、NODL4、GH3.1、ENODL2、ENOD93的表达, 强化了土壤中固氮微生物的功能, 促进了豆科作物的生物固氮。a: competition of maize for soil nitrogen alleviates nitrogen blockage to promote nodule nitrogen fixation in faba bean; b: Maize root exudates promote flavonoid synthesis in faba bean, increase nodulation, and stimulate nitrogen fixation after enhanced gene expression; maize root exudates significantly increase the expression of genes of CFI, NODL4, GH3.1, ENODL2 and ENOD93 in faba bean roots, and stimulate the key soil microorganisms, which enhances nitrogen fixation of faba bean.
图 3 粮食作物和超富集植物间作缓解重金属毒害的作用机制(修改于郭思宇等[20])
Figure 3. Mechanisms of reducing heavy metal toxicity of crops and hyperaccumulators intercropping (Modified from GUO S Y, et al[20])
粮食作物和超富集作物间作, 根系分泌物中有机酸含量改变, 促进超富集作物对重金属的吸收, 降低粮食作物对重金属的吸收。In heavy metal hyperaccumulators/crops intercropping system, the content of organic acids in root exudates changes, the heavy metal uptake by hyperaccumulators is increased, the heavy metal uptake by crops is decreased.
表 1 根系分泌物介导种间相互作用实例
Table 1. Examples of interspecific interactions mediated by root exudes
根系分泌物作用 Root exudates effects 举例 Example 参考文献 Reference 根系分泌物通过促进养分吸收和利用驱动的种间促进作用
Interspecific facilitation via nutrient mobilization driven by root exudates难溶性土壤磷的活化与吸收
Mobilization and absorption of insoluble P in soils蚕豆/玉米间作, 蚕豆向根际释放质子、苹果酸和柠檬酸促进蚕豆、玉米对磷的吸收
In faba bean/maize intercropping, the roots of faba bean released carboxylates or proton to promote P uptake of faba bean and maize[24] 鹰嘴豆和小麦或玉米间作, 鹰嘴豆根分泌酸性磷酸酶促进作物对磷的获取
In maize/chickpea or wheat/chickpea intercropping, acid phosphatase released from chickpea roots promotes the P uptake of different crops[25-26] 增强豆科作物结瘤固氮作用
Improvement of nodulation and nitrogen fixation of legumes蚕豆/玉米间作, 玉米根系分泌物黄酮类化合物促进蚕豆结瘤固氮
Root exudates from maize include flavonoids improving the nodulation and nitrogen fixation of faba bean in faba bean/maize intercropping[27] 铁的吸收与活化
Mobilization and absorption of Fe花生/玉米间作, 玉米根系分泌的麦根酸类铁载体形成PS-Fe(Ⅲ)溶解Fe(Ⅲ), 被还原成花生吸收的Fe(Ⅱ)
In peanut/maize intercropping, phytosiderophores secreted by maize roots help to solubilize Fe (Ⅲ) in the form of Fe (Ⅲ)-PS complexes, which reduced to Fe (Ⅱ) and taken up by the peanut[36] 根系分泌物降低重金属毒害促进相邻作物生长
Root exudates reducing heavy metal toxicity and promoting the neighbor plants增强对Al3+的耐受性
Improvement of tolerance to Al3+ toxicity小麦、大麦、水稻根系通过释放柠檬酸、苹果酸、酚类化合物螯合游离的Al3+降低Al3+对于根系的毒害作用
Malate, citrate, and oxalate secretion has been demonstrated to chelate free Al3+ and mediate the Al tolerance of cereals including wheat, barley and rice[40-42] 超富集植物和粮食作物间作降低粮食作物对重金属的积累
The heavy metal uptake by crops is decreased in heavy metal hyperaccumulators / crops intercropping system龙葵和玉米间作, 龙葵根系分泌有机酸与Cd2+形成螯合物, 促进龙葵对Cd的吸收和富集, 降低玉米对Cd的吸收
Intercropping generally enhances low molecular weight organic acid secretion from the roots of nightshade to construct chelation with Cd2+, the heavy metal uptake by hyperaccumulators is increased and the heavy metal uptake by crops is decreased under nightshade/maize intercropping[45-46] 续断菊和玉米间作, 改变两种作物的根系分泌物中有机酸的种类和含量, 增加了续断菊对Cd的吸收和积累, 抑制了玉米Cd的积累
Intercropping of Sonchus asper/maize changes the types and amount of organic acids in root exudation, which increases Cd uptake and accumulation in S. asper but inhibits Cd accumulation in maize[39] 续断菊和玉米间作, 增加续断菊根系分泌柠檬酸和草酸的数量, 影响了植物体内Pb的累积
Intercropping of Sonchus asper/maize resulted in increasing of the citric acid and oxalic acid secreted by S. asper, which increased the uptake and accumulation of Pb in S. asper[47] 根系分泌物通过调控微生物群落促进相邻作物生长
Interspecific facilitation driven by root exudates regulating microbial community通过调控微生物群落抑制土传病害
Infection of soil borne diseases via regulating microbial community西瓜/水稻间作降低了尖孢镰刀菌的密度, 可防治西瓜枯萎病
Intercropping with aerobic rice suppressed Fusarium wilt in watermelon by reducing the density Fusarium oxysporum[52] 茴香与烟草、甜瓜、三七轮作通过根系分泌物抑制病菌, 显著抑制烟草黑胫病、甜瓜枯萎、三七根腐病等土传病害
The rotation of fennel with tobacco, melon and radix pseudo-ginseng can significantly decrease the incidence of tobacco black shank, melon root rot and radix pseudo-ginseng root rot through root exudates of fennel[53] 玉米/辣椒间作, 玉米根系分泌物中的抗菌物质有效抑制了辣椒疫病的传播
Antimicrobe compounds secreted by maize resulted in the inhibition of Phytophthora capsici disease in maize and pepper intercropping systems[54] 根系分泌物介导的植物种间化感作用
Plant interspecific allelopathy mediated by root exudates醌类化感物质
Quinones allelochemicals胡桃树的根系能够分泌化感物质萘醌及胡桃醌, 抑制相邻植物的生长
The napthoquinone and juglone are produced by root of black walnut, which can inhibit the growth of neighbouring plants[64] 黄酮类化感物质
Flavonoids allelochemicals水稻通过根分泌化感物质二萜内酯、环己烯酮和黄酮等, 抑制稻田杂草的生长
Rice roots secrete diterpenoid lactones, cyclohexanone and flavonoids to suppress weeds[65] 苯并恶嗪类化感物质
Benzoxazinoids allelochemicals小麦通过根系释放丁布化感物质抑制杂草生长
DIMBOA allelochemicals released by wheat roots inhibit weeds[69] 缓解自毒作用
Alleviation of autotoxicity杉木连续单作种植, 释放的化感物质环二肽因浓度增高, 产生自毒作用; 杉木与含笑一起种植, 缓解抑制作用
In continuous Chinese fir monocultures, Chinese fir trees produce and release a novel allelochemical cyclic dipeptide into the soil, resulting in autotoxicity, if Chinese fir is planted with Michelia figo the inhibition will be alleviated[76] 桃园内残留物含有大量的扁桃苷, 经土壤根际微生物和相关酶分解生成有毒的CN−, 对桃树产生自毒作用, 间作农作物可缓解自毒
The residues in the peach orchard contain a large amount of amygdalin, which is decomposed by soil rhizosphere microorganisms and related enzymes to produce toxic CN−, resulting in autotoxicity, the inhibition will be alleviated by intercropping with crops[77] 
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