Chaetomium uniseriatum Promotes Maize Growth by Accelerating Straw Degradation and Regulating the Expression of Hormone Responsive Genes

doi:10.11983/CBB21147

Abstract

Abstract: To explore the effect of Chaetomium uniseriatum on straw degradation and maize growth, C. uniseriatum was inoculated into pots planted with maize, with other conditions unchanged to ensure a single variable. The soil organic carbon, microbial biomass C/N, dissolved organic C/N content and enzymes activities were measured to assess the response of soil biochemical properties to C. uniseriatum inoculation at jointing and tasseling stage. The degradation rate of straw, aboveground biomass, SPAD value of leaves, root hormones and root transcriptomes were investigated to verify the influence of C. uniseriatum on the growth of maize. The soil nutrients content did not change significantly in inoculated treatments, while the activity of β-glucosidase (β-GC) decreased significantly. At tasseling stage, the aboveground biomass, SPAD value of leaves and degradation rate of straw were significantly enhanced in inoculated treatments as compared with the control. The contents of auxin (IAA) and zeatin (ZR) in maize roots were significantly lower than those in control. Transcriptome analysis of maize roots revealed that there were 990 differentially expressed genes (607 down regulated and 383 up regulated) between the two treatments. Five GO terms associated with regulation of plant hormones were enriched, and one hormone related pathway was enriched significantly (P value<0.05, Q value<0.05) according to KEGG annotation. Our study revealed that C. uniseriatum could improve maize growth by accelerating straw degradation and regulating the expression of hormone response genes in roots.

Key words: Chaetomium uniseriatum, transcriptome, phytohormone, straw degradation, soil nutrients

Li Yue, Hu Desheng, Tan Jinfang, Mei Hao, Wang Yi, Li Hui, Li Fang, Han Yanlai. Chaetomium uniseriatum Promotes Maize Growth by Accelerating Straw Degradation and Regulating the Expression of Hormone Responsive Genes[J]. Chinese Bulletin of Botany, 2022, 57(4): 422-433.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB21147

https://www.chinbullbotany.com/EN/Y2022/V57/I4/422

Figures/Tables 8

References 55

[1]	鲍士旦 (2000). 土壤农化分析(第3版). 北京: 中国农业出版社. pp. 25-38.
[2]	郭栋, 杜媚, 周宝元, 刘颖慧, 赵明 (2019). 玉米SAUR基因家族的鉴定与生物信息学分析. 植物遗传资源学报 20, 90-99.
[3]	何芳芳, 王海军, 王雪莹 (2020). 纤维素酶的研究进展. 造纸科学与技术 39(4), 1-8.
[4]	滕青云, 乐丽娜, 宋冰倩, 陈英 (2020). 植物TIR1/AFBs基因家族研究进展. 农业工程 10, 93-97.
[5]	Abdel-Azeem AM, Gherbawy YA, Sabry AM (2016). Enzyme profiles and genotyping of Chaetomium globosum isolates from various substrates. Plant Biosyst 150, 420-428. DOI URL
[6]	Allen HR, Ptashnyk M (2020). Mathematical modelling of auxin transport in plant tissues: flux meets signaling and growth. Bull Math Biol 82, 17. DOI URL
[7]	Anders S, Huber W (2010). Differential expression analysis for sequence count data. Genome Biol 11, R106. DOI URL
[8]	Archer SK, Shirokikh NE, Preiss T (2014). Selective and flexible depletion of problematic sequences from RNA-seq libraries at the cDNA stage. BMC Genomics 15, 401. DOI URL
[9]	Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000). Gene ontology: tool for the unification of biology. Nat Genet 25, 25-29. DOI PMID
[10]	Berendsen RL, Pieterse CMJ, Bakker PAHM (2012). The rhizosphere microbiome and plant health. Trends Plant Sci 17, 478-486. DOI PMID
[11]	Berhane M, Xu M, Liang ZY, Shi JL, Wei GH, Tian XH (2020). Effects of long-term straw return on soil organic carbon storage and sequestration rate in North China upland crops: a meta-analysis. Glob Change Biol 26, 2686-2701. DOI URL
[12]	Cañizares R, Benitez E, Ogunseitan OA (2011). Molecular analyses of β-glucosidase diversity and function in soil. Eur J Soil Biol 47, 1-8. DOI URL
[13]	Chen YN, Chen YR, Li YP, Wu YX, Zhu FZ, Zeng GM, Zhang JC, Li H (2018). Application of Fenton pretreatment on the degradation of rice straw by mixed culture of Phanerochaete chrysosporium and Aspergillus niger. Ind Crop Prod 112, 290-295. DOI URL
[14]	Fattorini L, Falasca G, Kevers C, Mainero Rocca L, Zadra C, Altamura MM (2009). Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers. Planta 231, 155-168. DOI PMID
[15]	Glickmann E, Dessaux Y (1995). A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61, 793-796. DOI URL
[16]	Guilfoyle TJ, Ulmasov T, Hagen G (1998). The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol Life Sci 54, 619-627. PMID
[17]	Jaroszuk-Ściseł J, Kurek E, Trytek M (2014). Efficiency of indoleacetic acid, gibberellic acid and ethylene synthesized in vitro by Fusarium culmorum strains with different effects on cereal growth. Biologia 69, 281-292. DOI URL
[18]	Jiang C, Song JZ, Zhang JZ, Yang Q (2017). New production process of the antifungal chaetoglobosin A using cornstalks. Braz J Microbiol 48, 410-418. DOI URL
[19]	Jiang XZ, Du JW, He RN, Zhang ZY, Qi F, Huang JZ, Qin L (2020). Improved production of majority cellulases in Trichoderma reesei by integration of cbh1gene grom Chaetomium thermophilum. Front Microbiol 11, 1633. DOI URL
[20]	Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008). KEGG for linking genomes to life and the environment. Nucleic Acids Res 36, D480-D484. DOI PMID
[21]	Kang SM, Khan AL, Waqas M, You YH, Kim JH, Kim JG, Hamayun M, Lee IJ (2014). Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9, 673-682. DOI URL
[22]	Kazan K, Manners JM (2009). Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14, 373-382. DOI URL
[23]	Khan AL, Shinwari ZK, Kim YH, Waqas M, Hamayun M, Kamran M, Lee IJ (2012). Role of endophyte Chaetomium globosum lk4 in growth of Capsicum annuum by producion of gibberellins and indole acetic acid. Pak J Bot 44, 1601-1607.
[24]	Laothanachareon T, Bunterngsook B, Suwannarangsee S, Eurwilaichitr L, Champreda V (2015). Synergistic action of recombinant accessory hemicellulolytic and pectinolytic enzymes to Trichoderma reesei cellulase on rice straw degradation. Bioresour Technol 198, 682-690. DOI URL
[25]	Leyser O (2005). Auxin distribution and plant pattern formation: how many angels can dance on the point of PIN? Cell 121, 819-822. DOI URL
[26]	Li F, Zhang SQ, Wang Y, Li Y, Li PP, Chen L, Jie XL, Hu DS, Feng B, Yue K, Han YL (2020). Rare fungus, Mortierella capitata, promotes crop growth by stimulating primary metabolisms related genes and reshaping rhizosphere bacterial community. Soil Biol Biochem 151, 108017. DOI URL
[27]	Li ZX, Zhang XR, Zhao YJ, Li YJ, Zhang GF, Peng ZH, Zhang JR (2018). Enhancing auxin accumulation in maize root tips improves root growth and dwarfs plant height. Plant Biotechnol J 16, 86-99. DOI URL
[28]	Liu G, Yu HY, Ma J, Xu H, Wu QY, Yang JH, Zhuang YQ (2015). Effects of straw incorporation along with microbial inoculant on methane and nitrous oxide emissions from rice fields. Sci Total Environ 518-519, 209-216. DOI URL
[29]	Liu HW, Brettell LE, Qiu ZG, Singh BK (2020). Microbiome-mediated stress resistance in plants. Trends Plant Sci 25, 733-743. DOI URL
[30]	Liu X, Zhou F, Hu GQ, Shao S, He HB, Zhang W, Zhang XD, Li LJ (2019). Dynamic contribution of microbial residues to soil organic matter accumulation influenced by maize straw mulching. Geoderma 333, 35-42. DOI URL
[31]	Manirakiza E, Ziadi N, St Luce M, Hamel C, Antoun H, Karam A (2019). Nitrogen mineralization and microbial biomass carbon and nitrogen in response to co-application of biochar and paper mill biosolids. Appl Soil Ecol 142, 90-98. DOI
[32]	Millevoi S, Vagner S (2010). Molecular mechanisms of eukaryotic pre-mRNA 3′ end processing regulation. Nucleic Acids Res 38, 2757-2774. DOI URL
[33]	Narukawa-Nara M, Nakamura A, Kikuzato K, Kakei Y, Sato A, Mitani Y, Yamasaki-Kokudo Y, Ishii T, Hayashi KI, Asami T, Ogura T, Yoshida S, Fujioka S, Kamakura T, Kawatsu T, Tachikawa M, Soeno K, Shimada Y (2016). Aminooxy-naphthylpropionic acid and its derivatives are inhibitors of auxin biosynthesis targeting L-tryptophan aminotransferase: structure-activity relationships. Plant J 87, 245-257. DOI URL
[34]	Ortiz J, Soto J, Fuentes A, Herrera H, Meneses C, Arriagada C (2019). The endophytic fungus Chaetomium cupreum regulates expression of genes involved in the tolerance to metals and plant growth promotion in eucalyptus globulus roots. Microorganisms 7, 490. DOI URL
[35]	Park JH, Choi GJ, Jang KS, Lim HK, Kim HT, Cho KY, Kim JC (2005). Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. FEMS Microbiol Lett 252, 309-313. DOI URL
[36]	Pedraza-Zapata DC, Sánchez-Garibello AM, Quevedo-Hidalgo B, Moreno-Sarmiento N, Gutiérrez-Rojas I (2017). Promising cellulolytic fungi isolates for rice straw degradation. J Microbiol 55, 711-719. DOI PMID
[37]	Raza W, Mei XL, Wei Z, Ling N, Yuan J, Wang JC, Huang QW, Shen QR (2017). Profiling of soil volatile organic compounds after long-term application of inorganic, organic and organic-inorganic mixed fertilizers and their effect on plant growth. Sci Total Environ 607-608, 326-338. DOI URL
[38]	Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002). The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34, 1309-1315. DOI URL
[39]	Sato M, Winter JM, Kishimoto S, Noguchi H, Tang Y, Watanabe K (2016). Combinatorial generation of chemical diversity by redox enzymes in chaetoviridin biosynthesis. Org Lett 18, 1446-1449 DOI URL
[40]	Shanthiyaa V, Saravanakumar D, Rajendran L, Karthikeyan G, Prabakar K, Raguchander T (2013). Use of Chaetomium globosum for biocontrol of potato late blight disease. Crop Prot 52, 33-38. DOI URL
[41]	Siegel-Hertz K, Edel-Hermann V, Chapelle E, Terrat S, Raaijmakers JM, Steinberg C (2018). Comparative microbiome analysis of a Fusarium wilt suppressive soil and a Fusarium wilt conducive soil from the Châteaurenard region. Front Microbiol 9, 568. DOI PMID
[42]	Singh A, Sharma S (2002). Composting of a crop residue through treatment with microorganisms and subsequent vermicomposting. Bioresour Technol 85, 107-111. DOI URL
[43]	Timmusk S, Wagner EGH (1999). The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant Microbe Interact 12, 951-959. DOI URL
[44]	Uddling J, Gelang-Alfredsson J, Piikki K, Pleijel H (2007). Evaluating the relationship between leaf chlorophyll concentration and SPAD-502 chlorophyll meter readings. Photosynth Res 91, 37-46. DOI URL
[45]	Vance ED, Brookes PC, Jenkinson DS (1987). Anextraction method for measuring soil microbial biomass C. Soil Biol Biochem 19, 703-707. DOI URL
[46]	Wang B, Funakoshi D, Dalpé Y, Hamel C (2002). Phosphorus-32 absorption and translocation to host plants by arbuscular mycorrhizal fungi at low root-zone temperature. Mycorrhiza 12, 93-96. PMID
[47]	Wang R, Zhang HC, Sun LG, Qi GF, Chen S, Zhao XY (2017). Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Sci Rep 7, 343. DOI PMID
[48]	Wu JS, Joergensen RG, Pommerening B, Chaussod R (1990). Measurement of soil microbial biomass c by fumigation extraction—an automated procedure. Soil Biol Biochem 22, 1167-1169. DOI URL
[49]	Xu J, Han HF, Ning TY, Li ZJ, Lal R (2019). Long-term effects of tillage and straw management on soil organic carbon, crop yield, and yield stability in a wheat-maize system. Field Crop Res 233, 33-40. DOI URL
[50]	Yang HS, Zhou JJ, Weih M, Li YF, Zhai SL, Zhang Q, Chen WP, Liu J, Liu L, Hu SJ (2020). Mycorrhizal nitrogen uptake of wheat is increased by earthworm activity only under no-till and straw removal conditions. Appl Soil Ecol 155, 103672. DOI URL
[51]	Yang J, Kloepper JW, Ryu CM (2009). Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14, 1-4. DOI URL
[52]	Yun SI, Jeong CS, Chung DK, Choi HS (2001). Purification and some properties of a β-glucosidase from Trichoderma harzianum type C-4. Biosci Biotechnol Biochem 65, 2028-2032. DOI URL
[53]	Zhang Y, Yu XX, Zhang WJ, Lang DY, Zhang XJ, Cui GC, Zhang XH (2019). Interactions between endophytes and plants: beneficial effect of endophytes to ameliorate biotic and abiotic stresses in plants. J Plant Biol 62, 1-13. DOI
[54]	Zhao XL, Yuan GY, Wang HY, Lu DJ, Chen XQ, Zhou JM (2019). Effects of full straw incorporation on soil fertility and crop yield in rice-wheat rotation for silty clay loamy cropland. Agronomy 9, 133. DOI URL
[55]	Zhao XY, He XS, Xi BD, Gao RT, Tan WB, Zhang H, Li D (2016). The evolution of water extractable organic matter and its association with microbial community dynamics during municipal solid waste composting. Waste Manage 56, 79-87. DOI URL

Gene	log₂(FoldChange)	P value	Gene description
Zm00001d032724*	-1.541	0.000	Disease resistance RPP13-like protein 4
Zm00001d035172*	-0.901	0.041	Disease resistance protein RPM1
Zm00001d030888	-0.327	0.227	Probable disease resistance protein
Zm00001d054090	-1.297	0.259	Protein enhanced disease resistance 2
Zm00001d041343	-0.278	0.307	Probable disease resistance protein
Zm00001d043197	-0.549	0.349	Probable disease resistance protein
Zm00001d052992	-0.251	0.368	Disease resistance protein RPM1
Zm00001d021491	-0.267	0.370	Disease resistance RPP13-like protein 4
Zm00001d041358	-1.208	0.394	NBS-LRR disease resistance protein-like
Zm00001d043233	-0.239	0.407	Disease resistance gene analog PIC21
Zm00001d031711	-0.529	0.435	Disease resistance gene analog PIC15
Zm00001d032510	-0.632	0.473	Putative disease resistance RPP13-like protein 1
Zm00001d006873	-0.329	0.517	Disease resistance response protein-like; protein
Zm00001d007776	-0.298	0.519	Disease resistance protein RGA2
Zm00001d024681	-0.599	0.547	Disease resistance protein RPM1
Zm00001d017954	-0.179	0.554	Disease resistance protein RPM1
Zm00001d049121	-0.296	0.582	Disease resistance protein RPM1
Zm00001d035973	-0.159	0.601	Protein enhanced disease resistance 2
Zm00001d048663	-0.180	0.611	Disease resistance protein RGA2
Zm00001d024977	-0.376	0.623	Disease resistance protein RPM1
Zm00001d014654	-0.130	0.651	Disease resistance protein RPM1
Zm00001d034555	-0.179	0.653	Disease resistance protein RPM1
Zm00001d006755	-0.260	0.658	Disease resistance RPP13-like protein 4
Zm00001d021564	-0.936	0.681	Disease resistance protein RPM1
Zm00001d014876	-0.104	0.726	Disease resistance RPP13-like protein 4
Zm00001d037648	-0.090	0.753	Disease resistance protein RPP13
Zm00001d024975	-0.111	0.756	Disease resistance protein RPM1
Zm00001d048639	-0.147	0.762	Disease resistance protein RPM1
Zm00001d007935	-0.593	0.781	Disease resistance response protein 206
Zm00001d007630	-0.051	0.844	Disease resistance protein RPS2
Zm00001d023923	-0.056	0.872	Disease resistance protein RPM1
Zm00001d045512	-0.177	0.886	Putative disease resistance RPP13-like protein 3
Zm00001d044172	-0.022	0.903	SGT1 disease resistance protein homolog1
Zm00001d045335	-0.027	0.916	Putative disease resistance RPP13-like protein 1
Zm00001d052389	-0.094	0.923	Disease resistance protein RPM1
Zm00001d048637	-0.062	0.950	Disease resistance RPP13-like protein 4
Zm00001d048635	-0.282	0.971	Disease resistance protein RPM1
Zm00001d032166	-0.016	0.975	Protein enhanced disease resistance 2
Zm00001d053244	-0.002	1.000	Disease resistance protein (TIR-NBS class)
Zm00001d048613	-0.031	1.000	Disease resistance protein RGA2

Gene	log₂(FoldChange)	P value	Gene description
Zm00001d032724*	-1.541	0.000	Disease resistance RPP13-like protein 4
Zm00001d035172*	-0.901	0.041	Disease resistance protein RPM1
Zm00001d030888	-0.327	0.227	Probable disease resistance protein
Zm00001d054090	-1.297	0.259	Protein enhanced disease resistance 2
Zm00001d041343	-0.278	0.307	Probable disease resistance protein
Zm00001d043197	-0.549	0.349	Probable disease resistance protein
Zm00001d052992	-0.251	0.368	Disease resistance protein RPM1
Zm00001d021491	-0.267	0.370	Disease resistance RPP13-like protein 4
Zm00001d041358	-1.208	0.394	NBS-LRR disease resistance protein-like
Zm00001d043233	-0.239	0.407	Disease resistance gene analog PIC21
Zm00001d031711	-0.529	0.435	Disease resistance gene analog PIC15
Zm00001d032510	-0.632	0.473	Putative disease resistance RPP13-like protein 1
Zm00001d006873	-0.329	0.517	Disease resistance response protein-like; protein
Zm00001d007776	-0.298	0.519	Disease resistance protein RGA2
Zm00001d024681	-0.599	0.547	Disease resistance protein RPM1
Zm00001d017954	-0.179	0.554	Disease resistance protein RPM1
Zm00001d049121	-0.296	0.582	Disease resistance protein RPM1
Zm00001d035973	-0.159	0.601	Protein enhanced disease resistance 2
Zm00001d048663	-0.180	0.611	Disease resistance protein RGA2
Zm00001d024977	-0.376	0.623	Disease resistance protein RPM1
Zm00001d014654	-0.130	0.651	Disease resistance protein RPM1
Zm00001d034555	-0.179	0.653	Disease resistance protein RPM1
Zm00001d006755	-0.260	0.658	Disease resistance RPP13-like protein 4
Zm00001d021564	-0.936	0.681	Disease resistance protein RPM1
Zm00001d014876	-0.104	0.726	Disease resistance RPP13-like protein 4
Zm00001d037648	-0.090	0.753	Disease resistance protein RPP13
Zm00001d024975	-0.111	0.756	Disease resistance protein RPM1
Zm00001d048639	-0.147	0.762	Disease resistance protein RPM1
Zm00001d007935	-0.593	0.781	Disease resistance response protein 206
Zm00001d007630	-0.051	0.844	Disease resistance protein RPS2
Zm00001d023923	-0.056	0.872	Disease resistance protein RPM1
Zm00001d045512	-0.177	0.886	Putative disease resistance RPP13-like protein 3
Zm00001d044172	-0.022	0.903	SGT1 disease resistance protein homolog1
Zm00001d045335	-0.027	0.916	Putative disease resistance RPP13-like protein 1
Zm00001d052389	-0.094	0.923	Disease resistance protein RPM1
Zm00001d048637	-0.062	0.950	Disease resistance RPP13-like protein 4
Zm00001d048635	-0.282	0.971	Disease resistance protein RPM1
Zm00001d032166	-0.016	0.975	Protein enhanced disease resistance 2
Zm00001d053244	-0.002	1.000	Disease resistance protein (TIR-NBS class)
Zm00001d048613	-0.031	1.000	Disease resistance protein RGA2