Soil microbial legacy drives crop diversity advantage: linking ecological plant-soil feedback with agricultural intercropping

Although the importance of the soil microbiome in mediating plant
community structures and functions has been increasingly emphasized in
ecological studies, the biological processes driving crop diversity
overyielding remain unexplained in agriculture. Based on the plant-soil
feedback (PSF) theory and method, we quantified how much soil microbes
contributed to intercropping overyielding and detected which microbial
groups mediated this effect. Soils were collected as inocula and sequenced
from a unique 10-year field experiment, consisting of monoculture,
intercropping and rotation planted with wheat (Triticum aestivum), maize
(Zea mays) or faba bean (Vicia faba). A PSF study was conducted to test
microbial effects on three crops’ growth in monoculture or intercropping.
In wheat & faba bean (W&F) and maize & faba bean
(M&F) systems, soil microbes drove intercropping overyielding
compared to monoculture, with 28-51% of the overyielding contributed by
microbial legacies. The overyielding effects resulted from negative PSFs
in both systems, as crops, in particular faba bean grew better in soils
conditioned by other crops than itself. Moreover, faba bean grew better in
soils from intercropping or rotation than from the average of
monocultures, indicating a strong positive legacy effect of multispecies
cropping systems. However, with positive PSF and negative legacy benefit
effect of intercropping/rotation, we did not observe significant
overyielding in the W&M system. With more bacterial and fungal
dissimilarities by metabarcoding in heterospecific than its own soil, the
better it improved faba bean growth. More detailed analysis showed faba
bean monoculture soil accumulated more putative pathogens with higher
Fusarium relative abundance and more Fusarium oxysporum gene copies by
qPCR, while in heterspecific soils, there was less pathogenetic effects
when cereals were engaged. Further analysis in maize/faba bean
intercropping also showed an increase of rhizobia relative abundance.
Synthesis and applications. Our results demonstrate a soil
microbiome-mediated advantage in intercropping through suppression of the
negative PSF of pathogens and increasing beneficial microbes. As microbial
mediation of overyielding is context-dependent, we conclude that the
dynamics of both beneficial and pathogenic microbes should be considered
in designing cropping systems for sustainable agriculture, particularly
including combinations of legumes and cereals.

尽管生态学研究中愈发重视土壤微生物组（soil microbiome）在调控植物群落结构与功能中的核心作用，但农业领域中驱动作物多样性超产的生物学机制仍未被阐明。本研究基于植物-土壤反馈（plant-soil feedback, PSF）理论与方法，量化了土壤微生物对作物间作超产的贡献程度，并解析了介导该效应的微生物类群。研究依托一项独特的10年定位田间试验采集土壤接种物并进行测序，该试验设置了单作、间作与轮作三种种植模式，供试作物为普通小麦（Triticum aestivum）、玉米（Zea mays）与蚕豆（Vicia faba）。随后开展PSF试验，探究土壤微生物对单作与间作模式下三种供试作物生长的影响。在小麦-蚕豆（W&F）与玉米-蚕豆（M&F）种植体系中，相较于单作模式，土壤微生物可显著驱动作物间作超产，其中28%-51%的超产效应由微生物遗留效应介导。两种体系中的间作超产效应均源于负向PSF：相较于自身根际土壤，供试作物（尤其是蚕豆）在其他作物根际驯化的土壤中生长更佳。此外，蚕豆在间作或轮作体系土壤中的生长表现优于单作体系土壤的平均水平，这表明多物种种植体系具有显著的正向微生物遗留效应。但在小麦-玉米（W&M）体系中，由于PSF为正向且间作/轮作的遗留效益为负，未观测到显著的间作超产效应。宏条形码（metabarcoding）分析显示，相较于同种作物根际土壤，异源土壤中细菌与真菌群落的相异程度更高，且该相异程度越高，越能促进蚕豆的生长。进一步的细节分析表明，蚕豆单作土壤中积累了更多潜在病原菌：通过定量PCR（qPCR）检测发现，该土壤中镰孢菌属（Fusarium）的相对丰度更高，且尖孢镰孢菌（Fusarium oxysporum）的基因拷贝数更多；而在异源土壤中，当伴生作物为谷类作物时，病原菌的致病效应显著减弱。针对玉米-蚕豆间作体系的后续分析还发现，根瘤菌（rhizobia）的相对丰度显著提升。研究结论与应用启示：本研究结果证实，土壤微生物组可通过抑制病原菌的负向PSF效应并富集有益微生物，从而赋予作物间作生长优势。鉴于微生物对间作超产的调控效应具有情境依赖性，本研究认为，在构建可持续农业种植体系（尤其是豆科与谷类作物的间作组合）时，应同时考量有益微生物与病原菌的群落动态变化。