Skip to main content

Advertisement

Log in

Transcriptome analysis reveals metabolic alteration due to consecutive monoculture and abiotic stress stimuli in Rehamannia glutinosa Libosch

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

We deeply investigated the mechanism underlying metabolic regulation in response to consecutive monoculture (replanting disease) and different abiotic stresses that unfolded the response mechanism to consecutive monoculture problem through RNA-seq analysis.

Abstract

The consecutive monoculture problem (CMP) resulted of complex environmental stresses mediated by multiple factors. Previous studies have noted that multiple stress factors in consecutive monoculture soils or plants severely limited the interpretation of the critical molecular mechanism, and made a predict that the specifically responding factor was autotoxic allelochemicals. To identify the specifically responding genes, we compared transcriptome changes in roots of Rehamannia glutinosa Libosch using consecutive monoculture, salt, drought, and ferulic acid as stress factors. Comparing with normal growth, 2502, 2672, 2485, and 1956 genes were differentially expressed in R. glutinosa under consecutive monoculture practice, salt, drought, and ferulic acid stress, respectively. In addition, 510 genes were specifically expressed under consecutive monoculture, which were not present under the other stress conditions. Integrating the biological and enrichment analyses of the differentially expressed genes, the result demonstrated that the plants could alter enzyme genes expression to reconstruct the complicated metabolic pathways, which used to tolerate the CMP and abiotic stresses. Furthermore, most of the affected pathway genes were closely related to secondary metabolic processes, and the influence of consecutive monoculture practice on the transcriptome genes expression profile was very similar to the profile under salt stress and then to the profile under drought stress. The outlined schematic diagram unfolded the putative signal regulation mechanism in response to the CMP. Genes that differentially up- or down-regulated under consecutive monoculture practice may play important roles in the CMP or replanting disease in R. glutinosa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

DEG:

Differentially expressed gene

CMP:

Consecutive monoculture problem

FP:

First year planting

SP:

Second year planting

SAP:

NaCl stress-treated plants

DP:

Drought stress-treated plants

FAP:

Ferulic acid treated plants

vs:

Versus

GO:

Gene ontology

CYP:

Cytochrome P450

UGT:

Uridine diphosphate glycosyl transferases

RPKM:

Per million mapped sequence reads

FDR:

False discovery rate

QCl:

Quality control

KEGG:

Kyoto encyclopedia of genes and genomes

SEA:

Singular enrichment analysis

EC:

Enzyme Commission

MVA:

Mevalonate

MEP:

Methylerythritol phosphate

HMGR:

Hydroxymethylglutaryl-CoA reductase

GPPS:

Geranyldiphosphate synthase

FPPS:

Farnesyldiphosphate synthase

GGPPS:

Geranylgeranyldiphosphate synthase

SQS:

Squalene synthase

SE:

Squalene monooxygenase

CAS:

Cycloartenol synthase

SMT2:

24-Methylene sterol C-methyl transferase

DWF5:

7-Dehydrocholesterol reductase

DWF1:

Delta24-sterol reductase

AACT:

Acetyl-CoA C-acetyl transferase

FK:

Delta 14-sterol reductase

BRs:

Sitosteroland brassinosteroids

CYP716A52V2:

B-Amyrin 28-oxidase

References

  • Babu PR, Rao KV, Reddy VD (2013) Structural organization and classification of cytochrome P450 genes in flax (Linum usitatissimum L.). Gene 513(1):156–162

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151(4):2006–2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9(1):26–32

    Article  CAS  PubMed  Google Scholar 

  • Beck JG, Mathieu D, Loudet C, Buchoux S, Dufourc EJ (2007) Plant sterols in “rafts”: a better way to regulate membrane thermal shocks. FASEB J 21(8):1714–1723

    Article  CAS  PubMed  Google Scholar 

  • Bourgaud F, Gravot A, Milesi S, Gontier E (2001) Production of plant secondary metabolites: a historical perspective. Plant Sci 161(5):839–851

    Article  CAS  Google Scholar 

  • Carland F, Fujioka S, Nelson T (2010) The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Plant Physiol 153(2):741–756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329(1–2):1–25

    Article  CAS  Google Scholar 

  • Christoph AS, Tanja R, Silvia S, Christoph L, Meinhart HZ, Duilio A, Adelbert B, Felix R, Wolfgang E (2003) Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy. Phytochem Rev 2:3–16

    Article  Google Scholar 

  • Devarenne TP, Ghosh A, Chappell J (2002) Regulation of squalene synthase, a key enzyme of sterol biosynthesis, in tobacco. Plant Physiol 129(3):1095–1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-lnduced phenylpropanoid metabolism. Plant cell 7(7):1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ginzberg IT, Fogelman M, Demirel E, Mweetwa U, Tokuhisa AM, J. Veilleux, R. E (2012) Induction of potato steroidal glycoalkaloid biosynthetic pathway by overexpression of cDNA encoding primary metabolism HMG-CoA reductase and squalene synthase. Planta 235(6):1341–1353

    Article  CAS  PubMed  Google Scholar 

  • Gong L, Zhang HX, Gan XY, Zhang L, Chen YC, Nie FJ, Shi L, Li M, Guo ZQ, Zhang GH, Song YX (2015) Transcriptome profiling of the potato (Solanum tuberosum L.) plant under drought stress and water-stimulus conditions. PLoS One 10(5):e0128041

    Article  PubMed  PubMed Central  Google Scholar 

  • Gressel J, Hanafi A, Head G, Marasas W, Obilana B, Ochanda J, Souissi T, Tzotzos G (2004) Major heretofore intractable biotic constraints to African food security that may be amenable to novel biotechnological solutions. Crop Prot 23(8):661–689

    Article  Google Scholar 

  • Griebel T, Zeier J (2010) A role for b-sitosterol to stigmasterol conversion in plant–pathogen interactions. Plant J 63(2):254–268

    Article  CAS  PubMed  Google Scholar 

  • Haralampidis K, Trojanowska M, Osbourn AE (2002) Biosynthesis of triterpenoid saponins in plants. Adv Biochem Eng Biotechnol 75(75):31–49

    CAS  PubMed  Google Scholar 

  • Holmberg N, Harker M, Gibbard CL, Wallace AD, Clayton JC, Rawlins S, Hellyer A, Safford R (2002) Sterol C-24 methyltransferase type 1 controls the flux of carbon into sterol biosynthesis in tobacco seed. Plant Physiol 130(1):303–311. doi:10.1104/pp.004226

    Article  Google Scholar 

  • Jaleel CA, Manivannan P, Kishorekumar A, Sankar B, Gopi R, Somasundaram R, Panneerselvam R (2007a) Alterations in osmoregulation, antioxidant enzymes and indole alkaloid levels in Catharanthus roseus exposed to water deficit. Colloids Surf B Biointerfaces 59(2):150–157

    Article  CAS  PubMed  Google Scholar 

  • Jaleel CA, Manivannan P, Sankar B, Kishorekumar A, Gopi R, Somasundaram R, Panneerselvam R (2007b) Induction of drought stress tolerance by ketoconazole in Catharanthus roseus is mediated by enhanced antioxidant potentials and secondary metabolite accumulation. Colloids Surf B Biointerfaces 60(2):201–206

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Hong MK, Choi H, Moon HS, Lee HJ (2015) Chemopreventive effects of korean red ginseng extract on rat hepatocarcinogenesis. J Cancer 6(1):1–8

    Article  PubMed  PubMed Central  Google Scholar 

  • Kobayashi M, Nagasaki H, Garcia V, Just D, Bres C, Mauxion JP, Le PM, Brunel D, Suda K, Minakuchi Y (2014) Genome-wide analysis of intraspecific DNA polymorphism in ‘Micro-Tom’, a model cultivar of tomato (Solanum lycopersicum). Plant Cell Physiol 55(2):445–454

    Article  CAS  PubMed  Google Scholar 

  • Lao S, Huang X, Huang H, Liu C, Zhang C, Bao Y (2015) Genomic and transcriptomic insights into the cytochrome P450 monooxygenase gene repertoire in the rice pest Brown planthopper, Nilaparvata lugens. Genomics 106(5):301–309

    Article  CAS  PubMed  Google Scholar 

  • Li ZF, Yang YQ, Xie DF, Zhu LF, Zhang ZG, Lin WX (2012) Identification of autotoxic compounds in fibrous roots of Rehmannia (Rehmannia glutinosa Libosch.). PLoS One 7(1):e28806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li MJ, Yang YH, Chen XJ, Wang FQ, Lin WX, Yi YJ, Zeng L, Yang SY, Zhang ZY (2013a) Transcriptome/degradome-wide identification of R. glutinosa miRNAs and their targets: the role of miRNA activity in the replanting disease. PLoS One 8 (7):e68531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YF, Wang Y, Tang Y, Kakani VG, Mahalingam R (2013b) Transcriptome analysis of heat stress response in switchgrass (Panicum virgatum L.). BMC Plant Biol 13:153

    Article  PubMed  PubMed Central  Google Scholar 

  • Loto I, Gutierrez MS, Barahona S, Sepulveda D, Martinez-Moya P, Baeza M, Cifuentes V, Alcaino J (2012) Enhancement of carotenoid production by disrupting the C22-sterol desaturase gene (CYP61) in Xanthophyllomyces dendrorhous. BMC Microbiol 12(1):235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittapelli SR, Maryada SK, Khareedu VR, Vudem DR (2014) Structural organization, classification and phylogenetic relationship of cytochrome P450 genes in Citrus clementina and Citrus sinensis. Tree Genet Genomes 10(2):399–409

    Article  Google Scholar 

  • Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628

    Article  CAS  PubMed  Google Scholar 

  • Nelson D, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66(1):194–211

    Article  CAS  PubMed  Google Scholar 

  • Nelson DR, Ming R, Alam M, Schuler MA (2008) Comparison of cytochrome P450 genes from six plant genomes. Trop Plant Biol 1(3–4):216–235

    Article  CAS  Google Scholar 

  • Petra ES, William JB, Dietrich W (1994) Nod factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulaton in soybean root exudate. Mol Plant Microbe Interact 7(3):384–390

    Article  Google Scholar 

  • Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6(11):1720–1731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reuter JA, Spacek DV, Snyder MP (2015) High-throughput sequencing technologies. Mol Cell 58(4):586–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen MJ, Chen L, Cao HB (2013) Study on trace elements in Rehmnnia Glutinosa Libosch. by principal component analysis and clustering analysis. Agric Sci Technol 14(12):1764–1768

    Google Scholar 

  • Singh AK, Dwivedi V, Rai A, Pal S, Reddy SG, Rao DK, Shasany AK, Nagegowda DA (2015) Virus-induced gene silencing of Withania somnifera squalene synthase negatively regulates sterol and defence-related genes resulting in reduced withanolides and biotic stress tolerance. Plant Biotechnol J 13(9):1287–1299

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Takahashi S, Watanabe R, Fukushima Y, Fujita N, Noguchi A, Yokoyama R, Nishitani K, Nishino T, Nakayama T (2006) An isoflavone conjugate-hydrolyzing beta-glucosidase from the roots of soybean (Glycine max) seedlings: purification, gene cloning, phylogenetics, and cellular localization. J Biol Chem 281(40):30251–30259

    Article  CAS  PubMed  Google Scholar 

  • Szakiel A, Pączkowski C, Henry M (2010) Influence of environmental abiotic factors on the content of saponins in plants. Phytochem Rev 10(4):471–491

    Article  Google Scholar 

  • Szalma SJ, Buckler ES, Snook ME, McMullen MD (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theor Appl Genet 110(7):1324–1333

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Nakamura Y, Asami T, Yoshida S, Matsuo T, Okamoto S (2003) Physiological roles of brassinosteroids in early growth of Arabidopsis: brassinosteroids have a synergistic relationship with gibberellin as well as auxin in light-grown hypocotyl elongation. J Plant Growth Regul 22(3):259–271

    Article  CAS  Google Scholar 

  • Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol 138(2):1117–1125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol Biochem 40(7):1971–1974

    Article  CAS  Google Scholar 

  • Villar E, Klopp C, Noirot C, Novaes E, Kirst M, Plomion C, Gion JM (2011) RNA-Seq reveals genotype-specific molecular responses to water deficit in eucalyptus. BMC Genomics 12:538–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant cell 24(3):842–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waisundara VY, Huang MQ, Hsu A, Huang DJ, Tan BKH (2008) Characterization of the anti-diabetic and anti-oxidant effects of Rehmannia glutinosa in streptozotocin-induced diabetic Wistar rats. Am J Chin Med 36(6):1083–1104

    Article  CAS  PubMed  Google Scholar 

  • Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139(2):822–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132(1):44–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Senthil-Kumar M, Ryu CM, Kang L, Mysore KS (2012) Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiol 158(4):1789–1802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JL, Meng XL, Lu RH, Wu C, Luo YT, Yan X, Li XJ, Kong XH, Nie GX (2015) Effects of Rehmannia glutinosa on growth performance, immunological parameters and disease resistance to aeromonas hydrophila in common carp (Cyprinus carpio L.). Aquaculture 435:293–300

    Article  Google Scholar 

  • Weston LA, Ryan PR, Watt M (2012) Mechanisms for cellular transport and release of allelochemicals from plant roots into the rhizosphere. J Exp Bot 63(9):3445–3454

    Article  CAS  PubMed  Google Scholar 

  • Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64(1):3–19

    Article  CAS  PubMed  Google Scholar 

  • Wink M (2013) Evolution of secondary metabolites in legumes (Fabaceae). S Afr J Bot 89:164–175

    Article  CAS  Google Scholar 

  • Wu LK, Wang HB, Zhang ZX, Lin R, Zhang ZY, Lin WX (2011) Comparative metaproteomic analysis on consecutively Rehmannia glutinosa-monocultured rhizosphere soil. PLoS One 6(5):e20611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu LK, Li ZF, Li J, Khan MA, Huang WM, Zhang ZY, Lin WX (2013) Assessment of shifts in microbial community structure and catabolic diversity in response to Rehmannia glutinosa monoculture. Appl Soil Ecol 67:1–9

    Article  Google Scholar 

  • Wu DD, Liu X, Qiu HZ, Zhang WM, Wang YF, Wang D, Shen QR (2015a) Effects of continuous potato cropping on salt accumulation and ion composition in soil. J Gansu Agric Univ 50(2):40–45

    CAS  Google Scholar 

  • Wu LK, Wang JY, Huang WM, Wu HM, Chen J, Yang YQ, Zhang ZY, Lin WX (2015b) Plant-microbe rhizosphere interactions mediated by Rehmannia glutinosa root exudates under consecutive monoculture. Sci Rep 5:15871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu LK, Wu HM, Chen J, Wang JY, Lin WX (2016) Microbial community structure and its temporal changes in Rehmannia glutinosa rhizospheric soils monocultured for different years. Eur J Soil Biol 72:1–5

    Article  Google Scholar 

  • Xuan TD, Shinkichi T, Khanh TD, Min CI (2005) Biological control of weeds and plant pathogens in paddy rice by exploiting plant allelopathy: an overview. Crop Prot 24(3):197–206

    Article  Google Scholar 

  • Yang YH, Li MJ (2016) DNA methylation in Rehmannia glutinosa roots suffering from replanting disease. Int J Agric Biol 18(1):160–167

    Article  CAS  Google Scholar 

  • Yang YH, Li MJ, Chen XJ, Wang PF, Wang FQ, Lin WX, Yi YJ, Zhang ZW, Zhang ZY (2014a) De novo characterization of the Rehmannia glutinosa leaf transcriptome and analysis of gene expression associated with replanting disease. Mol Breed 34(3):905–915

    Article  CAS  Google Scholar 

  • Yang YH, Li MJ, Li XY, Chen XJ, Lin WX, Zhang ZY (2014b) Transcriptome-wide identification of the genes responding to replanting disease in Rehmannia glutinosa L. roots. Mol Biol Rep 42(5):881–892

    Article  PubMed  Google Scholar 

  • Yang Y, Liu B, Du X, Li P, Liang B, Cheng X, Du L, Huang D, Wang L, Wang S (2015) Complete genome sequence and transcriptomics analyses reveal pigment biosynthesis and regulatory mechanisms in an industrial strain, Monascus purpureus YY-1. Sci Rep 5:8331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZL, Wang WQ (2010) Progress on formation mechanism and controlmeasurements of continuous cropping obstacles in plants. J Biol 27(5):69–72

    Google Scholar 

  • Zhang D, Wen XS, Wang XY, Shi M, Zhao Y (2009) Antidepressant effect of Shudihuang on mice exposed to unpredictable chronic mild stress. J Ethnopharmacol 123(1):55–60

    Article  PubMed  Google Scholar 

  • Zhang ZY, Li GL, Niu MM, Fan HM, Li J, Lin WX (2011a) Responses of physiological ecology and quality evaluation of Rehmannia gltinosa in continuous cropping. China J Chin Mater Med 36(9):1133–1136

    Google Scholar 

  • Zhang ZY, Lin WX, Yang YH, Chen H, Chen XJ (2011b) Effects of consecutively monocultured Rehmannia glutinosa L. on diversity of fungal community in rhizospheric soil. Agric Sci China 10(9):1374–1384

    Article  Google Scholar 

  • Zhang ZY, li MJ, Chen XJ, Wu LK, Li J, Wang FQ, Li ZF, Guo GY, Lin WX (2013) Research advancement and control strategy of consecutive monoculture problem of Rehmannia glutinosa L.. Modern Chin Med 15(1):38–44

    Google Scholar 

  • Zhu GJ, Wang MD, Wu ZW, Sun FL, Jia XC (2007) Analysis of potential allelochemicals in soils around rhizosphere of Rehmannia glutinosa Libosch. by GC–MS. Henan Sci 25(2):255–257

    Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (Nos. 81274022, 81573538, 81503193, 81403042, and 31271674), the Key Scientific Research Project of the higher Education Institutions of Fujian Province of China (No. JK2015013), and Fujian-Taiwan Joint Innovative Center for Germplasm Resources and cultivation of crop (FJ 2011 Program, No. 2015-75, China).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhongyi Zhang.

Ethics declarations

Conflict of interest

The authors have declared no conflict of interest.

Additional information

Communicated by Chun-Hai Dong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 5568 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tian, Y., Feng, F., Zhang, B. et al. Transcriptome analysis reveals metabolic alteration due to consecutive monoculture and abiotic stress stimuli in Rehamannia glutinosa Libosch. Plant Cell Rep 36, 859–875 (2017). https://doi.org/10.1007/s00299-017-2115-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-017-2115-2

Keywords

Navigation