Please wait a minute...
Journal of Integrative Agriculture  2021, Vol. 20 Issue (7): 1819-1831    DOI: 10.1016/S2095-3119(20)63355-X
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Transcriptome analysis for understanding the mechanism of dark septate endophyte S16 in promoting the growth and nitrate uptake of sweet cherry
WU Fan-lin1*, QU De-hui3*, TIAN Wei1, WANG Meng-yun1, CHEN Fei-yan1, LI Ke-ke1, SUN Ya-dong1, SU Ying-hua4, YANG Li-na5, SU Hong-yan1, WANG Lei2 
1 Key Laboratory of Molecular Module-Based Breeding of High Yield and Abiotic Resistant Plants in Universities of Shandong, School of Agriculture, Ludong University, Yantai 264025, P.R.China
2 College of Life Sciences, Ludong University, Yantai 264025, P.R.China
3 State Key Laboratory of Microbial Metabolism and School of Life Sciences & Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, P.R.China
4 State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an 271018, P.R.China
5 Department of Genetics and Cell Biology, Basic Medical College, Qingdao University, Qingdao 266071, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      


Sweet cherry is one of the most popular fresh fruits in the world.  Previously, we isolated a soilborne dark septate endophyte (DSE) strain, S16, which promoted the growth of Gisela 5 sweet cherry rootstock.  However, little is known about the molecular mechanism of the effect of S16 on the growth of sweet cherry.  In this study, the physiological parameters and transcript profiles of sweet cherry roots were analyzed under S16 treatment compared with a control to elucidate the molecular mechanisms of the effect of this strain on sweet cherry growth.  After inoculation with S16, sweet cherry seedlings exhibited more vigorous growth.  Moreover, we identified 4 249 differentially expressed genes (DEGs) between S16-treated plants and the control.  Many of the DEGs are involved in pathways related to plant growth, such as cellular metabolic and plant hormone pathways.  Additionally, some genes involved in nitrate regulation were also enriched; and these genes may be involved in the regulation of nitrate uptake in plants.  Physiological index detection demonstrated that S16 could improve the nitrate assimilation of sweet cherry via NO3 transporters. This RNA-seq dataset provides comprehensive insight into the transcriptomic landscape to reveal the molecular mechanisms whereby the DSE influences the growth of sweet cherry.
Keywords:  sweet cherry        dark septate endophyte        RNA-seq        growth        NO3 transporters  
Received: 05 March 2020   Accepted:
Fund: This study was supported by the National Natural Science Foundation of China (31570649), the Key Research and Development Program of Yantai City, Shandong Province, China (2019XDHZ089), the Natural Science Foundation of Shandong Province, China (ZR2019PC052 and 2017C03), and the Key Research and Development Program of Shandong Province, China (2019GSF107091, 2019GSF109114, 2018YYSP004 and 2018GNC110028).
Corresponding Authors:  Correspondence SU Hong-yan, E-mail: suhongyan66; WANG Lei, E-mail:    
About author:  WU Fan-lin, Mobile: +86-15965152366, E-mail: wufanlin1990;* These authors contributed equally to this study.

Cite this article: 

WU Fan-lin, QU De-hui, TIAN Wei, WANG Meng-yun, CHEN Fei-yan, LI Ke-ke, SUN Ya-dong, SU Ying-hua, YANG Li-na, SU Hong-yan, WANG Lei. 2021. Transcriptome analysis for understanding the mechanism of dark septate endophyte S16 in promoting the growth and nitrate uptake of sweet cherry. Journal of Integrative Agriculture, 20(7): 1819-1831.

Ballistreri G, Continella A, Gentile A, Amenta M, Fabroni S,  Rapisarda P. 2013. Fruit quality and bioactive compounds relevant to human health of sweet cherry (Prunus avium L.) cultivars grown in Italy. Food Chemistry, 140, 630–638.
Baltruschat H, Fodor J, Harrach B D, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel K H, Schafer P, Schwarczinger I, Zuccaro A, Skoczowski A. 2008. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist, 180, 501–510.
Barrow J R. 2003. Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza, 13, 239–247.
Boudsocq S, Niboyet A, Lata J C, Raynaud X, Loeuille N, Mathieu J, Blouin M, Abbadie L, Barot S. 2012. Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? American Naturalist, 180, 60–69.
Brautigam A, Gagneul D, Weber A P. 2007. High-throughput colorimetric method for the parallel assay of glyoxylic acid and ammonium in a single extract. Analytical Biochemistry, 362, 151–153.
Fature S, Cliquet J, Thephany G, Boucaud J. 1998. Nitrogen assimilation in Lolium perenne colonized by the arbuscular mycorrhizal fungus Glomus fasciculatum. New Phytologist, 138, 411–417.
Govindarajulu M, Pfeffer P E, Jin H, Abubaker J, Douds D D, Allen J W, Bucking H, Lammers P J, Shachar-Hill Y. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature, 435, 819–823.
Gray W M. 2004. Hormonal regulation of plant growth and development. PLoS Biology, 2, E311–E311.
Högberg P, Granström A, Johansson T, Lundmark-Thelin A, Näsholm T. 1986. Plant nitrate reductase activity as an indicator of availability of nitrate in forest soils. Canadian Journal of Forest Research, 16, 1165–1169.
Harrison M J. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology, 59, 19–42.
Hui F, Liu J, Gao Q, Lou B. 2015. Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. Journal of Environmental Sciences, 37, 184–191.
Johnson J M, Alex T, Oelmüller R. 2014. Piriformospora indica: The versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. Journal of Tropical Agriculture, 52, 103–122.
Khan A L, Lee I J. 2013. Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biolology, 13, 86.
Li L, Liu X, Peijnenburg W J, Zhao J, Chen X, Yu J, Wu H. 2012. Pathways of cadmium fluxes in the root of the halophyte Suaeda salsa. Ecotoxicology Environmental Safety, 75, 1–7.
Mandyam K G, Jumpponen A. 2014. Mutualism-parasitism paradigm synthesized from results of root-endophyte models. Frontiers in Microbiology, 5, 776.
Newsham K K. 2011. A meta-analysis of plant responses to dark septate root endophytes. New Phytologist, 190, 783–793.
Ogawa T, Fukuoka H, Yano H, Ohkawa Y. 1999. Relationships between nitrite reductase activity and genotype-dependent callus growth in rice cell cultures. Plant Cell Reports, 18, 576–581.
Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology, 6, 763–775.
Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson A G, Escobar M A. 2010. Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environment, 33, 1486–1501.
Seith B, Setzer B, Flaig H, Mohr H. 1994. Appearance of nitrate reductase, nitrite reductase and glutamine synthetase in different organs of the Scots pine (Pinus sylvestris) seedling as affected by light, nitrate and ammonium. Physiologia Plantarum, 91, 419–426.
Sukumar P, Legue V, Vayssieres A, Martin F, Tuskan G A, Kalluri U C. 2013. Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. Plant Cell Environment, 36, 909–919.
Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N. 2001. At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant Journal, 27, 407–415.
Temple S J, Vance C P, Stephen Gantt J. 1998. Glutamate synthase and nitrogen assimilation. Trends in Plant Science, 3, 51–56.
Wang L, Zhou Q, Ding L, Sun Y. 2008. Effect of cadmium toxicity on nitrogen metabolism in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator. Journal of Hazardous Materials, 154, 818–825.
Waqas M, Khan A L, Kamran M, Hamayun M, Kang S M, Kim Y H, Lee I J. 2012. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules, 17, 10754–10773.
von Wittgenstein N J, Le C H, Hawkins B J, Ehlting J. 2014. Evolutionary classification of ammonium, nitrate, and peptide transporters in land plants. BMC Evolutionary Biology, 14, 11.
Zhang C, Yin L, Dai S. 2009. Diversity of root-associated fungal endophytes in Rhododendron fortunei in subtropical forests of China. Mycorrhiza, 19, 417–423.
Zhang Y, Zhang S, Wang M, Bai F, Liu X. 2010. High diversity of the fungal community structure in naturally-occurring Ophiocordyceps sinensis. PLoS ONE, 5, e15570.
Zhang Y, Zhang Y, Liu M, Shi X, Zhao Z. 2008. Dark septate endophyte (DSE) fungi isolated from metal polluted soils: their taxonomic position, tolerance, and accumulation of heavy metals in vitro. Jouranl of  Microbiology, 46, 624–632.
[1] WANG Li-xin, WANG Lin-xia, ZHANG Meng-ling, QU Ying-yue, YUAN Ye, Ehsan SADEGHNEZHAD, GAO Meng-jiao, ZHAO Ruo-yu, QI Chao-feng, GUO Xiao-xue, ZHU Wen-hui, LI Rui-mei, DAI Li, LIU Meng-jun, LIU Zhi-guo. A cyclic effect of cAMP and calcium signaling contributes to jujube growth and development[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2094-2110.
[2] XIE Jiao, CAO Qi, WANG Wen-jun, ZHANG Hong-yan, DENG Bing. Understanding changes in volatile compounds and fatty acids of Jincheng orange peel oil at different growth stages using GC–MS[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2282-2294.
[3] HOU Qian-dong, HONG Yi, WEN Zhuang, SHANG Chun-qiong, LI Zheng-chun, CAI Xiao-wei, QIAO Guang, WEN Xiao-peng. Molecular characterization of the SAUR gene family in sweet cherry and functional analysis of PavSAUR55 in the process of abscission[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1720-1739.
[4] DONG Shi-man, XIAO Liang, LI Zhi-bo, SHEN Jie, YAN Hua-bing, LI Shu-xia, LIAO Wen-bin, PENG Ming. A novel long non-coding RNA, DIR, increases drought tolerance in cassava by modifying stress-related gene expression[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2588-2602.
[5] LÜ Jing, Satyabrata NANDA, CHEN Shi-min, MEI Yang, HE Kang, QIU Bao-li, ZHANG You-jun, LI Fei, PAN Hui-peng.

A survey on the off-target effects of insecticidal double-stranded RNA targeting the Hvβ´COPI gene in the crop pest Henosepilachna vigintioctopunctata through RNA-seq [J]. >Journal of Integrative Agriculture, 2022, 21(9): 2665-2674.

[6] WANG Jie, ZHANG Qi, Astrid Lissette BARRETO SÁNCHEZ, ZHU Bo, WANG Qiao, ZHENG Mai-qing, LI Qing-he, CUI Huan-xian, WEN Jie, ZHAO Gui-ping. Transcriptome analysis of the spleen of heterophils to lymphocytes ratio-selected chickens revealed their mechanism of differential resistance to Salmonella[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2372-2383.
[7] LI Si-ping, ZENG Lu-sheng, SU Zhong-liang. Wheat growth, photosynthesis and physiological characteristics under different soil Zn levels[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1927-1940.
[8] PAN Wen-jing, HAN Xue, HUANG Shi-yu, YU Jing-yao, ZHAO Ying, QU Ke-xin, ZHANG Ze-xin, YIN Zhen-gong, QI Hui-dong, YU Guo-long, ZHANG Yong, XIN Da-wei, ZHU Rong-sheng, LIU Chun-yan, WU Xiao-xia, JIANG Hong-wei, HU Zhen-bang, ZUO Yu-hu, CHEN Qing-shan, QI Zhao-ming. Identification of candidate genes related to soluble sugar contents in soybean seeds using multiple genetic analyses[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1886-1902.
[9] DU Qing-guo, YANG Juan, Shah SYED MUHAMMAD SADIQ, YANG Rong-xin, YU Jing-juan, LI Wen-xue. Comparative transcriptome analysis of different nitrogen responses in low-nitrogen sensitive and tolerant maize genotypes[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2043-2055.
[10] ZHOU Nian-bing, ZHANG jun, FANG Shu-liang, WEI Hai-yan, ZHANG Hong-cheng. Effects of temperature and solar radiation on yield of good eating-quality rice in the lower reaches of the Huai River Basin, China[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1762-1774.
[11] LI Yong-ping, LIU Tian-jia, LUO Hui-feng, LIU Sheng-cai . The transcriptional landscape of cultivated strawberry (Fragaria×ananassa) and its diploid ancestor (Fragaria vesca) during fruit development[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1540-1553.
[12] ZHANG Zhe, CHEN Zi-tao, DIAO Shu-qi, YE Shao-pan, WANG Jia-ying, GAO Ning, YUAN Xiao-long, CHEN Zan-mou, ZHANG Hao, LI Jia-qi. Identifying the complex genetic architecture of growth and fatness traits in a Duroc pig population[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1607-1614.
[13] CHEN Li-li, WANG Hao-ying, GONG Xiao-chen, ZENG Zhao-hai, XUE Xu-zhang, HU Yue-gao. Transcriptome analysis reveals effects of red and blue lightemitting diodes (LEDs) on the growth, chlorophyll fluorescence and endogenous plant hormones of potato (Solanum tuberosum L.) plantlets cultured in vitro[J]. >Journal of Integrative Agriculture, 2021, 20(11): 2914-2931.
[14] GONG Xiao-dong, LIU Yu-wei, BI Huan-huan, YANG Xiao-rong, HAN Jian-min, DONG Jin-gao, GU Shou-qin. StKU80, a component in the NHEJ repair pathway, is involved in mycelial morphogenesis, conidiation, appressorium development, and oxidative stress reactions in Exserohilum turcicum[J]. >Journal of Integrative Agriculture, 2021, 20(1): 147-158.
[15] WANG Chuan-long, XING Guan-zhong, WANG Li-sai, LI Su-fen, ZHANG Li-yang, LU Lin, LUO Xu-gang, LIAO Xiu-dong . Effects of selenium source and level on growth performance, antioxidative ability and meat quality of broilers[J]. >Journal of Integrative Agriculture, 2021, 20(1): 227-235.
No Suggested Reading articles found!