Tea plant–legume intercropping simultaneously improves soil fertility and tea quality by changing Bacillus species composition

Zhi Huang , Chunhong Cui , Yajun Cao , Jinghui Dai , Xiaoyue Cheng , Shaowei Hua , Wentao Wang , Yu Duan , Evangelos Petropoulos , Hui Wang , Lixiang Zhou , Wanping Fang , Zengtao Zhong

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac046

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac046 DOI: 10.1093/hr/uhac046
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Tea plant–legume intercropping simultaneously improves soil fertility and tea quality by changing Bacillus species composition
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Abstract

The tea plant is an economically important crop in China, but long-term monoculture and substantial chemical nitrogen fertilizer input cause soil acidification, which in turn affects the nutrient supply and tea quality. Intercropping has drawn more attention in tea gardens because this pattern is expected to improve soil fertility and tea quality and change the soil microbial community composition. However, the roles of some key microorganisms in rhizosphere soils have not been well characterized. Here, a “soybean in summer and smooth vetch in winter” strategy was used in a tea garden to investigate the effects of intercropped legumes on soil fertility, tea quality, and potential changes in beneficial bacteria such as Bacillus. Our data showed that when soybeans were turned into the soil, the intercropping system exhibited higher soil organic matter (SOM), total nitrogen (TN), tea quality indices, and expression of the Camellia sinensis glutamine synthetase gene (CsGS). Notably, intercropping significantly affected the bacterial communities, decreasing the relative abundance of Bacillus but increasing its absolute abundance. Bacillus amyloliquefaciens BM1 was isolated from intercropped soil and showed outstanding plant growth-promoting (PGP) properties when co-inoculated with rhizobia. In winter, intercropping with smooth vetch had a beneficial effect on soil properties and tea quality. Co-inoculation with strain BM1 and Rhizobium leguminosarum Vic5 on smooth vetch (Vicia villosa) produced huge improvements in SOM, TN, and tea leaf quality, which were accompanied by the highest level of amino acids and the lowest levels of polyphenols and caffeine (p < 0.05). Our findings demonstrate that intercropping with some legumes in the tea garden is a strategy that increases SOM, TN, and tea quality, and the optional use of some PGP Bacillus species produces an amplification effect.

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Zhi Huang, Chunhong Cui, Yajun Cao, Jinghui Dai, Xiaoyue Cheng, Shaowei Hua, Wentao Wang, Yu Duan, Evangelos Petropoulos, Hui Wang, Lixiang Zhou, Wanping Fang, Zengtao Zhong. Tea plant–legume intercropping simultaneously improves soil fertility and tea quality by changing Bacillus species composition. Horticulture Research, 2022, 9 (1) : uhac046 DOI:10.1093/hr/uhac046

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References

[1]

Silva LS, Seabra AR, Leitão JN, Carvalho HG . Possible role of glutamine synthetase of the prokaryotic type (GSI-like) in nitrogen signaling in Medicago truncatula . Plant Sci. 2015; 240: 98-108.

[2]

Rana NK, Mohanpuria P, Yadav SK . Cloning and characterization of a cytosolic glutamine synthetase from Camellia sinensis (L.) O. Kuntze that is upregulated by ABA, SA, and H2O2 . Mol Biotechnol. 2008; 39: 49-56.

[3]

Wu Y, Li Y, Fu X et al. Three-dimensional spatial variability in soil microorganisms of nitrification and denitrification at row-transect scale in a tea field. Soil Biol Biochem. 2016; 103: 452-63.

[4]

Ma L, Chen H-j, Shan Y-j et al. Status and suggestions of tea garden fertilization on main green tea-producing counties in Zhengjiang Province. J Tea Sci. 2013; 33: 74-84.

[5]

Li Y, Li ZW, Arafat Y et al. Characterizing rhizosphere microbial communities in long-term monoculture tea orchards by fatty acid profiles and substrate utilization. Eur J Soil Biol. 2017; 81: 48-54.

[6]

Yang X-D, Ni K, Yuanzhi S et al. Effects of long-term nitrogen application on soil acidification and solution chemistry of a tea plantation in China. Agric Ecosyst Environ. 2018; 252: 74-82.

[7]

Wang Z, Geng Y, Liang T . Optimization of reduced chemical fertilizer use in tea gardens based on the assessment of related environmental and economic benefits. Sci Total Environ. 2020; 713: 136439.

[8]

Li J, Zhou Y, Zhou B et al. Habitat management as a safe and effective approach for improving yield and quality of tea (Camellia sinensis) leaves . Sci Rep. 2019; 9: 433.

[9]

Farooq TH, Kumar U, Mo J et al. Intercropping of peanut-tea enhances soil enzymatic activity and soil nutrient status at different soil profiles in subtropical southern China. Plan Theory. 2021; 10: 881.

[10]

Duan Y, Shang X, Liu G et al. Effects of soybean-tea intercropping on soil-available nutrients and tea quality. Acta Physiol Plant. 2019; 41: 140.

[11]

Wu T, Qin Y, Li M . Intercropping of tea (Camellia sinensis L.) and Chinese chestnut: variation in the structure of rhizosphere bacterial communities . J Soil Sci Plant Nutr. 2021; 21: 2178-90.

[12]

Ma YH, Fu SL, Zhang XP et al. Intercropping improves soil nutrient availability, soil enzyme activity and tea quantity and quality. Appl Soil Ecol. 2017; 119: 171-8.

[13]

Arafat Y, Wei X, Jiang Y et al. Spatial distribution patterns of root-associated bacterial communities mediated by root exudates in different aged ratooning tea monoculture systems. Int J Mol Sci. 2017; 18: 1727.

[14]

Gui H, Fan L, Wang D et al. Organic management practices shape the structure and associations of soil bacterial communities in tea plantations. Appl Soil Ecol. 2021; 163: 103975.

[15]

Li YC, Li Z, Li ZW et al. Variations of rhizosphere bacterial communities in tea (Camellia sinensis L.) continuous cropping soil by high-throughput pyrosequencing approach . J Appl Microbiol. 2016; 121: 787-99.

[16]

Shen F-T, Lin S-H . Priming effects of cover cropping on bacterial community in a tea plantation. Sustainability. 2021; 13: 4345.

[17]

Gardener BBMS . Ecology of bacillus and Paenibacillus spp. in agricultural systems . Phytopathology. 2004; 94: 1252-8.

[18]

Wen T, Yuan J, He X et al. Enrichment of beneficial cucumber rhizosphere microbes mediated by organic acid secretion. Hortic Res. 2020; 7: 154.

[19]

Arafat Y, Din IU, Tayyab M et al. 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. Front Plant Sci. 2020; 11: 601.

[20]

Korir H, Mungai NW, Thuita M et al. Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front Plant Sci. 2017; 8: 141.

[21]

Matse DT, Huang C-H, Huang Y-M, Yen M-Y . Effects of co-inoculation of rhizobium with plant growth promoting rhizobacteria on the nitrogen fixation and nutrient uptake of Trifolium repens on low phosphorus soil . J Plant Nutr. 2020; 43: 739-52.

[22]

Yang L, Lou J, Wang H et al. Use of an improved high-throughput absolute abundance quantification method to characterize soil bacterial community and dynamics. Sci Total Environ. 2018; 633: 360-71.

[23]

Props R, Kerckhof F-M, Rubbens P et al. Absolute quantification of microbial taxon abundances. ISME J. 2017; 11: 584-7.

[24]

Prest EI, El-Chakhtoura J, Hammes F et al. Combining flow cytometry and 16S rRNA gene pyrosequencing: a promising approach for drinking water monitoring and characterization. Water Res. 2014; 63: 179-89.

[25]

Lou J, Yang L, Wang H et al. Assessing soil bacterial community and dynamics by integrated high-throughput absolute abundance quantification. PeerJ. 2018; 6: e4514.

[26]

Wen B, Zhang X, Ren S et al. Characteristics of soil nutrients, heavy metals and tea quality in different intercropping patterns. Agrofor Syst. 2020; 94: 963-74.

[27]

Kermah M, Franke AC, Adjei-Nsiah S et al. Maize-grain legume intercropping for enhanced resource use efficiency and crop productivity in the Guinea savanna of northern Ghana. Field Crops Res. 2017; 213: 38-50.

[28]

Duan Y, Shang X, Liu G et al. The effects of tea plants-soybean intercropping on the secondary metabolites of tea plants by metabolomics analysis. BMC Plant Biol. 2021; 21: 482.

[29]

Fu H, Li H, Yin P et al. Integrated application of rapeseed cake and green manure enhances soil nutrients and microbial communities in tea garden soil. Sustainability. 2021; 13: 2967.

[30]

Rahav E, Giannetto MJ, Bar-Zeev E . Contribution of mono and polysaccharides to heterotrophic N2 fixation at the eastern Mediterranean coastline . Sci Rep. 2016; 6: 27858.

[31]

Li Y, Pan F, Yao H . Response of symbiotic and asymbiotic nitrogen-fixing microorganisms to nitrogen fertilizer application. J Soils Sediments. 2019; 19: 1948-58.

[32]

Zhou X, Zhang J, Pan D et al. P-Coumaric can alter the composition of cucumber rhizosphere microbial communities and induce negative plant-microbial interactions. Biol Fertil Soils. 2018; 54: 363-72.

[33]

Wang L, Huang D, Wang F et al. Bacterial communities in acid tea soils treated for 10 years with chemical vs. integrated fertilizers. Commun Soil Sci Plant Anal. 2019; 50: 307-20.

[34]

Pérez-García A, Romero D, de Vicente A . Plant protection and growth stimulation by microorganisms: biotechnological applications of bacilli in agriculture. Curr Opin Biotech. 2011; 22: 187-93.

[35]

Dame ZT, Rahman M, Islam T . Bacilli as source of agrobiotechnology: recent advances and future directions. Green Chem Lett Rev. 2021; 14: 246-71.

[36]

Wang Y-S, Liu J-C, Chen W-C, Yen J-H . Characterization of acetanilide herbicides degrading bacteria isolated from tea garden soil. Microb Ecol. 2008; 55: 435-43.

[37]

Wang X, Wang M, Xie X-G et al. An amplification-selection model for quantified rhizosphere microbiota assembly. Sci Bull. 2020; 65: 983-6.

[38]

Zhang ZJ, Qu Y, Li S et al. Soil bacterial quantification approaches coupling with relative abundances reflecting the changes of taxa. Sci Rep. 2017; 7: 4837.

[39]

Su X, Li G, Cotner JB et al. Long-term organic fertilization changes soil active bacterial composition and multifunctionality: RNA-based bacterial community and qPCR-based SmartChip analysis. J Soils Sediments. 2021; 21: 799-809.

[40]

Feng Y, Chen R, Hu J et al. Bacillus asahii comes to the fore in organic manure fertilized alkaline soils . Soil Biol Biochem. 2015; 81: 186-94.

[41]

Tilak KVBR, Ranganayaki N, Manoharachari C . Synergistic effects of plant-growth promoting rhizobacteria and rhizobium on nodulation and nitrogen fixation by pigeonpea (Cajanus cajan) . Eur J Soil Sci. 2006; 57: 67-71.

[42]

Han Q, Ma Q, Chen Y et al. Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean. ISME J. 2020; 14: 1915-28.

[43]

Masciarelli O, Llanes A, Luna V . A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol Res. 2014; 169: 609-15.

[44]

Sibponkrung S, Kondo T, Tanaka K et al. Co-inoculation of bacillus velezensis strain S141 and Bradyrhizobium strains promotes nodule growth and nitrogen fixation . Microorganisms. 2020; 8: 678.

[45]

Rajendran G, Sing F, Desai AJ, Archana G . Enhanced growth and nodulation of pigeon pea by co-inoculation of bacillus strains with rhizobium spp. Bioresour Technol. 2008; 99: 4544-50.

[46]

Ning J, DaXiang L, XianJingLi L et al. Stepwise identification of six tea (Camellia sinensis (L.)) categories based on catechins, caffeine, and theanine contents combined with fisher discriminant analysis . Food Anal Methods. 2016; 9: 1-9.

[47]

Bao SD . Agricultural Chemical Analysis of Soil . Beijing: China Agriculture Press; 2005.

[48]

Huang Z, Ruan S, Sun Y et al. Bacterial inoculants improved the growth and nitrogen use efficiency of Pyrus betulifolia under nitrogen-limited conditions by affecting the native soil bacterial communities. Appl Soil Ecol. 2022; 170: 104285.

[49]

Garbeva P, van Veen JA, van Elsas JD . Predominant bacillus spp. in agricultural soil under different management regimes detected via PCR-DGGE. Microb Ecol. 2003; 45: 302-16.

[50]

Caporaso JG, Kuczynski J, Stombaugh J et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7: 355-66.

[51]

Parks DH, Tyson GW, Hugenholtz P, Beiko RG . STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014; 30: 3123-4.

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