Abstract
Wheat seedlings are significantly impacted by the presence of bacteria. However, bacteria are unavoidably growing together with wheat. The study aimed to reveal wheat photosynthesis, phyllosphere bacterial community composition, and a shift in the bacterial community following different density treatments in a closed artificial ecosystem. Here, we report the relationship between photosynthesis and bacterial community in wheat seedlings for different planting densities. In this closed artificial ecosystem, a total of 30 phyla were detected, with 17 of them were simultaneously present in four treatments, under high light intensity and carbon dioxide growth environment. The key phyla detected include Firmicutes, Proteobacteria, and Bacteroidetes. We found that planting densities significantly impacted the photosynthetic characteristics of wheat and bacterial genetic biodiversity, but not on species composition of the bacterial community. Network analysis shows that the phyllosphere bacteria network structures were characterized by the clustering coefficient and modularity. Network for the 1000 plants/m2 treatment group exhibits the highest levels of average clustering coefficient but lowest modularity and number of modules, among all plant densities tested. In addition, the network for the 1200 plants/m2 treatment group exhibits the best characteristics in terms of net photosynthesis rate and intrinsic water use efficiency, higher complex phyllosphere community network structures, higher abundance of Corynebacterium, and more function of “Amino acid metabolism”, which encourages the plants to grow better. The findings presented in this work elucidated the role of plant density in the growth of phyllosphere bacteria during wheat seedlings and provided theoretical support for reasonable wheat density cultivation in closed artificial ecosystems and wheat field production.
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References
Ali N, Al-Awadhi H, Dashti N, Khanafer M, El-Nemr I, Sorkhoh N, Radwan SS (2015) Bioremediation of atmospheric hydrocarbons via bacteria naturally associated with leaves of higher plants. Int J Phytorem 17:1–35. https://doi.org/10.1080/15226514.2015.1045125
Alsanius BW, Bergstrand KJ, Hartmann R, Gharaie S, Wohanka W, Dorais M, Rosberg AK (2017) Ornamental flowers in new light: artificial lighting shapes the microbial phyllosphere community structure of greenhouse grown sunflowers (Helianthus annuus L.). Sci Hortic 216:234–247. https://doi.org/10.1016/j.scienta.2017.01.022
Alsanius BW, Karlsson M, Rosberg AK, Dorais M, Naznin MT, Khalil S, Bergstrand KJ (2019) Light and microbial lifestyle: the impact of light quality on plant-microbe interactions in horticultural production systems – a review. Hortic 5:1–24. https://doi.org/10.3390/horticulturae5020041
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Aßhauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinf 31:2882–2884. https://doi.org/10.1093/bioinformatics/btv287
Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. International AAAI Conference on Weblogs and Social Media. https://gephi.org/
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Carvalho SD, Castillo JA (2018) Influence of light on plant–phyllosphere interaction. Front Plant Sci 9:1482. https://doi.org/10.3389/fpls.2018.01482
Chávez-Romero Y, Navarro-Noya YE, Reynoso-Martínez SC, Sarria-Guzmán Y, Govaerts B, Verhulst N, Dendooven L, Luna-Guido M (2016) 16S metagenomics reveals changes in the soil bacterial community driven by soil organic C, N-fertilizer and tillage-crop residue management. Soil Tillage Res 159:1–8. https://doi.org/10.1016/j.still.2016.01.007
Chen S, Waghmode TR, Sun R, Kuramae E (2019) Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome 7:136. https://doi.org/10.1186/s40168-019-0750-2
da Silva TF, Vollú RE, Marques JM, Salles JF, Seldin L (2017) The bacterial community associated with rose-scented geranium (Pelargonium graveolens) leaves responds to anthracnose symptoms. Plant Soil 414:69–79. https://doi.org/10.1007/s11104-016-3102-z
Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Roschitzki R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. PNAS 106:16428–16433. https://doi.org/10.1073/pnas.0905240106
Dong C, Fu Y, Liu G, Liu H (2014) Low light intensity effects on the growth, photosynthetic characteristics, antioxidant capacity, yield and quality of wheat (Triticum aestivum L.) at different growth stages in BLSS. Adv Space Res 53:1557–1566. https://doi.org/10.1016/j.asr.2014.02.004
Dong C, Shao L, Wang M, Liu G, Liu H, Xie B, Li B, Fu Y, Liu H (2016) Wheat carbon dioxide responses in space simulations conducted at the Chinese Lunar Palace-1. Agron J 108:32–38. https://doi.org/10.2134/agronj15.0265
Dong C, Chu Z, Wang M, Qin Y, Yi Z, Liu H, Fu Y (2018) Influence of nitrogen source and concentrations on wheat growth and production inside “Lunar Palace-1”. Acta Astronaut 144:371–379. https://doi.org/10.1016/j.actaastro.2017.12.043
Fan K, Weisenhornc P, Gilbertc JA, Chua H (2018) Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biol Biochem 125:251–260. https://doi.org/10.1016/j.soilbio.2018.07.022
Fang XM, She HZ, Wang C, Liu XB, Li YS, Nie J, Ruan R, Wang T, Yi ZL (2018) Effects of fertilizer application rate and planting density on photosynthetic characteristics, yield and yield components in waxy wheat. Cereal Res Commun 46:1–11. https://doi.org/10.1556/0806.45.2017.058
Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46. https://doi.org/10.1146/annurev-ecolsys-102710-145039
Fu Y, Li L, Xie B, Dong C, Wang M, Jia B, Shao L, Dong Y, Deng S, Liu H, Liu G, Liu B, Hu D, Liu H (2016) How to establish a bioregenerative life support system for long-term crewed missions to the moon or Mars. Astrobiol 16:925–936. https://doi.org/10.1089/ast.2016.1477
Gao Y, Li Y, Zhang J, Liu W, Dang Z, Cao W, Qin Q (2009) Effects of mulch, n fertilizer, and plant density on wheat yield, wheat nitrogen uptake, and residual soil nitrate in a dryland area of China. Nutr Cycl Agroecosyst 85:109–121. https://doi.org/10.1007/s10705-009-9252-0
Giri S, Pati BR (2004) A comparative study on phyllosphere nitrogen fixation by newly isolated Corynebacterium sp. & Flavobacterium sp. and their potentialities as biofertilizer. Acta Microbiol Immunol Hung 51:47–56. https://doi.org/10.1556/AMicr.51.2004.1-2.3
Gopinath V, Meiswinkel TM, Wendisch VF, Nampoothiri KM (2011) Amino acid production from rice straw and wheat bran hydrolysates by recombinant pentose-utilizing Corynebacterium glutamicum. Appl Microbiol Biotechnol 92:985–996. https://doi.org/10.1007/s00253-011-3478-x
Gu L, Bai Z, Jin B, Hu Q, Wang H, Zhuang G, Zhang H (2010) Assessing the impact of fungicide enostroburin application on bacterial community in wheat phyllosphere. J Environ Sci 22:134–141. https://doi.org/10.1016/S1001-0742(09)60084-X
Gurdeep R, Coaker GL, Leveau JHJ (2013) New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348:1–10. https://doi.org/10.1111/1574-6968.12225
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Station Bull 347:357–359. https://doi.org/10.1016/S0140-6736(00)73482-9
Hu Q, Tan L, Gu S, Xiao Y, Xiong X, Zeng W, Feng K, Wei Z, Deng Y (2020) Network analysis infers the wilt pathogen invasion associated with non-detrimental bacteria. NPJ Biofilms Microbiomes 6:1–8. https://doi.org/10.1038/s41522-020-0117-2
Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314. https://doi.org/10.1080/10618600.1996.10474713
Karlsson I, Friberg H, Kolseth AK, Steinberg C, Persson P (2017) Organic farming increases richness of fungal taxa in the wheat phyllosphere. Mol Ecol 26:3424–3436. https://doi.org/10.1111/mec.14132
Knief C, Ramette A, Frances L, Alonso-Blanco C, Vorholt JA (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J 4:719–728. https://doi.org/10.1038/ismej.2010.9
Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, Mering C, Vorholt J (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390. https://doi.org/10.1038/ismej.2011.192
Kordyum E, Chapman D, Brykov V (2019) Plant cell development and aging may accelerate in microgravity. Acta Astronaut 157:157–161. https://doi.org/10.1016/j.actaastro.2018.12.036
Lambais MR, Crowley DE, Cury JC, Büll RC (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917–1917. https://doi.org/10.1126/science.1124696
Li P, Cheng Z, Ma B, Palta J, Kong H, Mo F, Wang J, Zhu Y, Lv G, Batool A, Bai X, Li F, Xiong Y (2014) Dryland wheat domestication changed the development of aboveground architecture for a well-structured canopy. PLoS One 9:e95825. https://doi.org/10.1371/journal.pone.0095825
Li YP, Li YY, Li DY, Wang SW, Zhang SQ (2017) Photosynthetic response of tetraploid and hexaploid wheat to water stress. Photosynthetica 55:454–466. https://doi.org/10.1007/s11099-016-0659-y
Liu TN, Wang ZL, Cai T (2016) Canopy apparent photosynthetic characteristics and yield of two spike-type wheat cultivars in response to row spacing under high plant density. PLoS One 11:e0148582. https://doi.org/10.1371/journal.pone.0148582
Liu L, Xia Y, Liu B, Chang C, Xiao L, Shen J, Tang L, Cao W, Zhu Y (2020) Individual and combined effects of jointing and booting low-temperature stress on wheat yield. Eur J Agron 113:1–10. https://doi.org/10.1016/j.eja.2019.125989
Ma D, Guo T, Zha F, Yue Y, Song X (2008) Effects of planting densities on microorganism population and soil enzyme activity in the rhizosphere of wheat. Chin J Acta Agric Boreali-Sinica 23:158–161. https://doi.org/10.7668/hbnxb.2008.03.037
Newman MEJ (2006) Modularity and community structure in networks. PNAS 103:8577–8582. https://doi.org/10.1073/pnas.0601602103
Pittol M, Scully E, Miller D, Durso L, Fiuza L, Valiati V (2018) Bacterial community of the rice floodwater using cultivation-independent approaches. Int J Microb 2018:1–13. https://doi.org/10.1155/2018/6280484
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. https://doi.org/10.1093/nar/gkm864
Qin Y, Fu Y, Dong C, Jia N, Liu H (2016) Shifts of microbial communities of wheat (Triticum aestivum L.) cultivation in a closed artificial ecosystem. Appl Microbiol Biotechnol 100:4085–4095. https://doi.org/10.1007/s00253-016-7317-y
Rahman MM, Flory E, Koyro HW, Abideen Z, Schikora A, Suarez C, Schnell S, Cardinale M (2018) Consistent associations with beneficial bacteria in the seed endosphere of barley (Hordeum vulgare L.). Syst Appl Microbiol 41:386–398. https://doi.org/10.1016/j.syapm.2018.02.003
Shen YZ, Guo SS, Ai WD, Tang YK (2014) Effects of light intensity and plant density on photosynthetic rate of wheat in enclosed system. Chin J Space Med Med Eng 27:54–58
Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium (VI) toxicity in legume plants: modulation effects of rhizobial symbiosis. Biomed Res Int 2018:1–13. https://doi.org/10.1155/2018/8031213
Stone BWG, Weingarten EA, Jackson C (2018) The role of the phyllosphere microbiome in plant health and function. Annu Plant Rev 2:1–24. https://doi.org/10.1002/9781119312994.apr0614
Sumi S, Suzuki Y, Matsuki T, Mise K, Kawamura T, Ito Y, Shimada Y, Watanabe E, Watanabe S, Toriyabe M, Takano H, Ueda K, Takano H (2019) Light-inducible carotenoid production controlled by a MarR-type regulator in Corynebacterium glutamicum. Sci Rep 9:1–15. https://doi.org/10.1038/s41598-019-49384-7
Vermeesch P, Resentini A, Garzanti E (2016) An R package for statistical provenance analysis. Sediment Geol 336:14–25. https://doi.org/10.1016/j.sedgeo.2016.01.009
Vorholt J (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840. https://doi.org/10.1038/nrmicro2910
Wang Z, Guo T, Wang H, Wang Y (2001) Effect of planting density on photosynthetic characteristics and grain yield of super-high-yield winter wheat at late growth stages. Chin J Triticeae Crops 21:64–67
Wheeler RM (2017) Agriculture for space: people and places paving the way. Open Agric 2:14–32. https://doi.org/10.1515/opag-2017-0002
Xiao Y, Liu J, Li H, Cao X, Xia X, He Z (2015) Lodging resistance and yield potential of winter wheat: effect of planting density and genotype. Front Agric Sci Eng 2:168–178. https://doi.org/10.15302/J-FASE-2015061
Yao H, Sun X, He C, Maitra P, Li X, Guo L (2019) Phyllosphere epiphytic and endophytic fungal community and network structures differ in a tropical mangrove ecosystem. Microbiome 7:1–15. https://doi.org/10.1186/s40168-019-0671-0
Yi Z, Cui J, Fu Y, Liu H (2020) Effect of different light intensity on physiology, antioxidant capacity and photosynthetic characteristics on wheat seedlings under high CO2 concentration in a closed artificial ecosystem. Photosynth Res 144:23–34. https://doi.org/10.1007/s11120-020-00726-x
Zervas A, Zeng Y, Madsen A, Hansen L (2019) Genomics of aerobic photoheterotrophs in wheat phyllosphere reveals divergent evolutionary patterns of photosynthetic genes in Methylobacterium spp. Genome Biol Evol 10:2895–2908. https://doi.org/10.1093/gbe/evz204
Zhang Y, Ji J, Guan C, Jin C, Li Q, Yan B, Wang G, Wang Y (2018) Screening of straw-degrading strains and their enzyme-producing conditions. Chin J Cellul Sci Technol 26:28–38
Zhou J, Deng Y, Luo F, He Z, Yang Y (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio 2:e00122–e00111. https://doi.org/10.1128/mBio.00122-11
Zwielehner J, Handschur M, Michaelsen A, Irez S, Demel M, Denner E, Haslberger A (2008) DGGE and real-time PCR analysis of lactic acid bacteria in bacterial communities of the phyllosphere of lettuce. Mol Nutr Food Res 5:614–623. https://doi.org/10.1002/mnfr.200700158
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This study was funded by the Pre-research Program on Manned Spaceflight (PR China, No. 020302) and National Natural Science Foundation of China (PR China, No. 31870852).
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ZY and HL conceived and designed research. ZY conducted experiments. ZY and JC analyzed data. YF guided most experiments. ZY and YF wrote the manuscript. All authors read and approved the manuscript.
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Yi, Z., Cui, J., Fu, Y. et al. The effect of wheat seedling density on photosynthesis may be associated with the phyllosphere microorganisms. Appl Microbiol Biotechnol 104, 10265–10277 (2020). https://doi.org/10.1007/s00253-020-10934-z
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DOI: https://doi.org/10.1007/s00253-020-10934-z