Skip to main content
Log in

Comparative study of the leaf transcriptomes and ionoms of Juglans regia and its wild relative species Juglans cathayensis

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Juglans regia ‘Yuanfeng’ is an elite walnut cultivar in China. Juglans cathayensis, a close relative species of Juglans regia originated from China, possesses some superior traits such as strong disease resistance and high fruit number per branch. So far, transcriptomes of either J. regia or J. cathayensis have not been studied and made available to public yet. In the present study, the transcriptomes of J. regia and J. cathayensis leaves were profiled using Illumina HiSeq 2000 platform. A total of 41,914 unigenes were obtained from the combined clean reads of J. regia and J. cathayensis with an average length of 1363 bp and 2529 differentially expressed genes (DEGs) were detected. Gene annotation analyses revealed that 38,483 unigenes (91.81%) were annotated in at least one of the five databases such as Gene Ontology (GO), etc. Meanwhile, the Ca, Mg, Fe, Zn, K and protein contents in the leaves of J. regia and J. cathayensis were compared and significant differences between J. regia and J. cathayensis in terms of the Ca, Mg, Fe and protein contents were discovered. In addition, DEGs associated with the Ca, Mg and Fe content variations between J. regia and J. cathayensis were investigated. Our comparative transcriptomes’ analysis between J. regia and J. cathayensis could provide a useful resource for genetic characterization and improvements of J. regia.

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

Similar content being viewed by others

Abbreviations

ACA:

Auto-inhibited Ca2+-ATPases

Atp2c:

Calcium-transporting ATPase-type 2C

CAX:

Cation/proton exchanger

Ca-P60A:

Calcium ATPase at 60A

DEG:

Differentially expressed gene

ECA:

Er-type Ca2+-ATPase

eggNOG:

Evolutionary genealogy of genes: Non-supervised Orthologous Groups

FRD:

Ferric reductase defective

GO:

Gene ontology

IRT:

Iron-regulated transporter

KEGG:

Kyoto Encyclopedia of Genes and Genomes

KO:

KEGG orthology

MHX:

Magnesium/proton exchanger

MTP:

Metal tolerance protein

NGS:

Next generation sequencing

nr:

Non-redundant database

NRAMP:

Natural resistance-associated macrophage protein

PPO:

Polyphenol oxidase

RNA-seq:

RNA sequencing

RPKM:

Reads per kb per million reads

SRA:

Short read archive

TPC:

Two-pore calcium channel

YSL:

Yellow stripe-like

References

  • Ahmad A, Shafique S, Shafique S (2013) Cytological and physiological basis for tomato varietal resistance against Alternaria alternata. J Sci Food Agric 93:2315–2322

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD (2013) Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat Protoc 8:1765–1786

    Article  PubMed  Google Scholar 

  • Araji S, Grammer TA, Gertzen R, Anderson SD, Mikulic-Petkovsek M, Veberic R, Phu ML, Solar A, Leslie CA, Dandekar AM, Escobar MA (2014) Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut. Plant Physiol 164:1191–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai WN, Wang WT, Zhang DY (2014) Contrasts between the phylogeographic patterns of chloroplast and nuclear DNA highlight a role for pollen-mediated gene flow in preventing population divergence in an East Asian temperate tree. Mol Phylogenet Evol 81:37–48

    Article  PubMed  Google Scholar 

  • Conn SJ, Conn V, Tyerman SD, Kaiser BN, Leigh RA, Gilliham M (2011) Magnesium transporters, MGT2/MRS2-1 and MGT3/MRS2-5, are important for magnesium partitioning within Arabidopsis thaliana mesophyll vacuoles. New Phytol 190:583–594

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347:749–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Escobar MA, Shilling A, Higgins P, Uratsu SL, Dandekar AM (2008) Characterization of polyphenol oxidase from walnut. J Am Soc Hortic Sci 133:852–858

    Google Scholar 

  • Fjellstrom RG, Parfitt DE (1994) Walnut (Juglans spp.) genetic diversity determined by restriction fragment length polymorphisms. Genome 37:690–700

    Article  CAS  PubMed  Google Scholar 

  • Furuichi T, Cunningham KW, Muto S (2001) A putative two pore channel AtTPC1 mediates Ca2+ flux in Arabidopsis leaf cells. Plant Cell Physiol 42:900–905

    Article  CAS  PubMed  Google Scholar 

  • Gaash R, Elazar M, Mizrahi K, Avramov-Mor M, Berezin I, Shaul O (2013) Phylogeny and a structural model of plant MHX transporters. BMC Plant Biol 13:75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gai JY (2000) Statistical methods for experiments. China agriculture press, Beijing (in Chinese)

    Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunn BF, Aradhya M, Salick JM, Miller AJ, Yongping Y, Lin L, Xian H (2010) Genetic variation in walnuts (Juglans regia and J. sigillata; Juglandaceae): species distinctions, human impacts, and the conservation of agrobiodiversity in Yunnan, China. Am J Bot 97:660–671

    Article  PubMed  Google Scholar 

  • Gur A, Zamir D (2004) Unused natural variation can lift yield barriers in plant breeding. PLoS Biol 2:1610–1615

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ladizinsky G (1985) Founder effect in crop-plant evolution. Econ Bot 39:191–199

    Article  Google Scholar 

  • Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247

    Article  CAS  PubMed  Google Scholar 

  • Lin YF, Liang HM, Yang SY, Boch A, Clemens S, Chen CC, Wu JF, Huang JL, Yeh KC (2009) Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182:392–404

    Article  CAS  PubMed  Google Scholar 

  • Ma QG, Zhang JP, Pei D (2011) Genetic analysis of walnut cultivars in China using fluorescent amplified fragment length polymorphism. Am Soc Hortic Sci 136:422–428

    CAS  Google Scholar 

  • Mammucari C, Gherardi G, Zamparo I, Raffaello A, Boncompagni S, Chemello F, Cagnin S, Braga A, Zanin S, Pallafacchina G, Zentilin L, Sandri M, De Stefani D, Protasi F, Lanfranchi G, Rizzuto R (2015) The mitochondrial calcium uniporter controls skeletal muscle trophism in vivo. Cell Rep 10:1269–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez ML, Labuckas DO, Lamarque AL, Maestri DM (2010) Walnut (Juglans regia L.): genetic resources, chemistry, by-products. J Sci Food Agric 90:1959–1967

    PubMed  Google Scholar 

  • Migeon A, Blaudez D, Wilkins O, Montanini B, Campbell MM, Richaud P, Thomine S, Chalot M (2010) Genome-wide analysis of plant metal transporters, with an emphasis on poplar. Cell Mol Life Sci 67:3763–3784

    Article  CAS  PubMed  Google Scholar 

  • Migocka M, Papierniak A, Maciaszczyk-Dziubińska E, Poździk P, Posyniak E, Garbiec A, Filleur S (2014) Cucumber metal transport protein MTP8 confers increased tolerance to manganese when expressed in yeast and Arabidopsis thaliana. J Exp Bot 65:5367–5384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mucchino C, Musci M (2014) Extraction of Al, Cu, Fe, Mn, Ni and Zn-polyphenol complexes from black tea infusions by Amberlite resins. J Sci Food Agric 94:2234–2238

    Article  CAS  PubMed  Google Scholar 

  • Periz G, Fortini ME (1999) Ca2+-ATPase function is required for intracellular trafficking of the Notch receptor in Drosophila. EMBO J 18:5983–5993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pineau C, Loubet S, Lefoulon C, Chalies C, Fizames C, Lacombe B, Ferrand M, Loudet O, Berthomieu P, Richard O (2012) Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Genet 8:e1003120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pires IS, Negrão S, Pentony MM, Abreu IA, Oliveira MM, Purugganan MD (2013) Different evolutionary histories of two cation/proton exchanger gene families in plants. BMC Plant Biol 13:97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, Jensen LJ, von Mering C, Bork P (2012) eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40:D284–D289

    Article  CAS  PubMed  Google Scholar 

  • Ricachenevsky FK, Menguer PK, Sperotto RA, Williams LE, Fett JP (2013) Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front Plant Sci 4:144

    PubMed  PubMed Central  Google Scholar 

  • Richter C, Dirks ME, Gronover CS, Prüfer D, Moerschbacher BM (2012) Silencing and heterologous expression of ppo-2 indicate a specific function of a single polyphenol oxidase isoform in resistance of dandelion (Taraxacum officinale) against Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 25:200–210

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Sze H, Liang F, Hwang I, Curran AC, Harper JF (2000) Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433–462

    Article  CAS  PubMed  Google Scholar 

  • Thipyapong P, Hunt MD, Steffens JC (2004) Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta 220:105–117

    Article  CAS  PubMed  Google Scholar 

  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci USA 97:4991–4996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Beek N, Patsatsi A, Gupta Y, Möller S, Freitag M, Lemcke S, Recke A, Zillikens D, Schmidt E, Ibrahim S (2015) A family with atypical Hailey Hailey disease—is there more to the under-lying Genetics than ATP2C1? PLoS ONE 10:e0121253

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87–96

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Li Y, Zhang YX, Chai TY (2013) Molecular cloning and characterization of a Brassica juncea yellow stripe-like gene, BjYSL7, whose overexpression increases heavy metal tolerance of tobacco. Plant Cell Rep 32:651–662

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Gu YQ, Hu Y, You FM, Dandekar AM, Leslie CA, Aradhya M, Dvorak J, Luo MC (2012) Characterizing the walnut genome through analyses of BAC end sequences. Plant Mol Biol 78:95–107

    Article  CAS  PubMed  Google Scholar 

  • Xiao J, Li J, Grandillo S, Ahn SN, Yuan L, Tanksley SD, McCouch SR (1998) Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Oryza rufipogon. Genetics 150:899–909

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Zhang MY, Gao L, Liu JF (2007) Development of new lines from walnut interspaces hybrids. Shandong Agric Sci 3:25–27 (in Chinese)

    Google Scholar 

  • Yordem BK, Conte SS, Ma JF, Yokosho K, Vasques KA, Gopalsamy SN, Walker EL (2011) Brachypodium distachyon as a new model system for understanding iron homeostasis in grasses: phylogenetic and expression analysis of Yellow Stripe-Like (YSL) transporters. Ann Bot 108:821–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You FM, Deal KR, Wang J, Britton MT, Fass JN, Lin D, Dandekar AM, Leslie CA, Aradhya M, Luo MC, Dvorak J (2012) Genome-wide SNP discovery in walnut with an AGSNP pipeline updated for SNP discovery in allogamous organisms. BMC Genomics 13:354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZY, Han JW, Jin Q, Wang Y, Pang XM, Li YY (2013) Development and characterization of new microsatellites for walnut (Juglans regia). Genet Mol Res 12:4723–4734

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Mr. Xuejun Ge of Lianchuang Walnut Plantation Co., Ltd., Suizhou, China, for providing experimental materials. Sequencing services were provided by Personal Biotechnology Co., Ltd., Shanghai, China. We also thank Tao Xu of Bionovogene Biotech Co., Ltd., Suizhou, China, for bioinformatics assistance. This work was jointly supported by the Demonstration Project of Forestry Science and Technology funded by the Central Government of China (the plan of Forestry Department of Hubei province, China, [2013]98) and the Natural Science Foundation of Hubei province, China (2012FFC031).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Shuifa Min or Jinbo Zhang.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by M Stobiecki.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, Z., Han, M., Hou, M. et al. Comparative study of the leaf transcriptomes and ionoms of Juglans regia and its wild relative species Juglans cathayensis . Acta Physiol Plant 39, 224 (2017). https://doi.org/10.1007/s11738-017-2504-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-017-2504-8

Keywords

Navigation