Soil Sickness in Aged Tea Plantation Is Associated With a Shift in Microbial Communities as a Result of Plant Polyphenol Accumulation in the Tea Gardens.

Sheng Lin,Zhaoying Cai,Yuhang Jiang,Yasir Arafat,Wenxiong Lin,Hanyu Zhao,Ting Chen,Xiangmin Lin,Muhammad Tayyab,Israr Ud Din

doi:10.3389/fpls.2020.00601

Sheng Lin, Zhaoying Cai + Show 8 more

Open Access

https://doi.org/10.3389/fpls.2020.00601

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Abstract

In conventional tea plantations, a large amount of pruned material returns to the soil surface, putting a high quantity of polyphenols into the soil. The accumulation of active allelochemicals in the tea rhizosphere and subsequent shift in beneficial microbes may be the cause of acidification, soil sickness, and regeneration problem, which may be attributed to hindrance of plant growth, development, and low yield in long-term monoculture tea plantation. However, the role of pruning leaf litter in soil sickness under consecutive tea monoculture is unclear. Here, we investigated soil samples taken from conventional tea gardens of different ages (2, 15, and 30 years) and under the effect of regular pruning. Different approaches including liquid chromatography–mass spectrometry (LC-MS) analysis of the leaf litter, metagenomic study of root-associated bacterial communities, and in vitro interaction of polyphenols with selected bacteria were applied to understand the effect of leaf litter-derived polyphenols on the composition and structure of the tea rhizosphere microbial community. Our results indicated that each pruning practice returns a large amount of leaf litter to each tea garden. LC-MS results showed that leaf litter leads to the accumulation of various allelochemicals in the tea rhizosphere, including epigallocatechin gallate, epigallocatechin, epicatechin gallate, catechin, and epicatechin with increasing age of the tea plantation. Meanwhile, in the tea garden grown consecutively for 30 years (30-Y), the phenol oxidase and peroxidase activities increased significantly. Pyrosequencing identified Burkholderia and Pseudomonas as the dominant genera, while plant growth-promoting bacteria, especially Bacillus, Prevotella, and Sphingomonas, were significantly reduced in the long-term tea plantation. The qPCR results of 30-Y soil confirmed that the copy numbers of bacterial genes per gram of the rhizosphere soil were significantly reduced, while that of Pseudomonas increased significantly. In vitro study showed that the growth of catechin-degrading bacteria (e.g., Pseudomonas) increased and plant-promoting bacteria (e.g., Bacillus) decreased significantly with increasing concentration of these allelochemicals. Furthermore, in vitro interaction showed a 0.36-fold decrease in the pH of the broth after 72 h with the catechin degradation. In summary, the increase of Pseudomonas and Burkholderia in the 30-Y garden was found to be associated with the accumulation of catechin substrates. In response to the long-term monoculture of tea, the variable soil pH along with the litter distribution negatively affect the population of plant growth-promoting bacteria (e.g., Sphingomonas, Bacillus, and Prevotella). Current research suggests that the removal of pruned branches from tea gardens can prevent soil sickness and may lead to sustainable tea production.

Highlights

Plant soil feedbacks can alter the composition and structure of the soil microbial community and nutrient homeostasis as a result of all the interactions between plants and soil organisms, affecting soil fertility and plant growth (Kaur et al, 2009; Bever et al, 2010; van de Voorde et al, 2012; Baxendale et al, 2014)
The objectives of this study were to inspect the impact of tea litter and its polyphenols on (a) root-related bacterial communities in terms of structure and composition, (b) ratooning or regeneration problems related to soil sickness, and (c) growth and quality parameters of tea plants in response to continuous tea cultivation
Tea plants grown in soil taken from different tea plantations (15-Y and 30-Y) showed weak growth, wilting, chlorosis, and regeneration obstacles compared to tea plants grown in the recently established tea garden (2-Y) soil (Figure 1)

Summary

Introduction

Plant soil feedbacks can alter the composition and structure of the soil microbial community and nutrient homeostasis as a result of all the interactions between plants and soil organisms, affecting soil fertility and plant growth (Kaur et al, 2009; Bever et al, 2010; van de Voorde et al, 2012; Baxendale et al, 2014). Long-term monoculture impedes the growth and production of many annual crops, trees, and shrubs in orchards and causes replanting and regeneration problems (Canals et al, 2005). It is pertinent to understand the mechanisms underlying soil sickness associated with long-term monoculture practice, to explore the allelochemical interaction with soil microbiota, and to provide a solution for maintaining a sustainable agro-ecosystem. Phenolics, being the most abundant plant metabolites, are thought to control the rates of soil organic matter decomposition and can be applied as a tool to evaluate the soil dynamics and ecosystem functioning (Min et al, 2015). The effects of soil microbiota are critical to the fate of plant phenolic compounds, including other potential allelochemicals found in the soil (Bever et al, 2010; Ehlers, 2011)

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