Skip to main content

Advertisement

SpringerLink
Log in

Influence of mitochondria on gene expression in a citrus cybrid

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

Abstract

The production of cybrids, combining nucleus of a species with alien cytoplasmic organelles, is a valuable method used for improvement of various crops. Several citrus cybrids have been created by somatic hybridization. These genotypes are interesting models to analyze the impact of cytoplasmic genome change on nuclear genome expression. Herein, we report genome-wide gene expression analysis in leaves of a citrus cybrid between C. reticulata cv ‘Willowleaf mandarin’ and C. limon cv ‘Eureka lemon’ compared with its lemon parent, using a Citrus 20K cDNA microarray. Molecular analysis showed that this cybrid possesses nuclear and chloroplast genomes of Eureka lemon plus mitochondria from Willowleaf mandarin and, therefore, can be considered as a lemon bearing foreign mitochondria. Mandarin mitochondria influenced the expression of a large set of lemon nuclear genes causing an over-expression of 480 of them and repression of 39 genes. Quantitative real-time RT–PCR further confirmed the credibility of microarray data. Genes over-expressed in cybrid leaves are predominantly attributed to the functional category “cellular protein metabolism” whereas in the down-regulated none functional category was enriched. Overall, mitochondria replacement affected different nuclear genes including particularly genes predicted to be involved in mitochondrial retrograde signaling. Mitochondria regulate all cell structures even chloroplast status. These results suggest that nuclear gene expression is modulated with respect to new information received from the foreign organelle, with the final objective to suit specific needs to ensure better cell physiological balance.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aharoni A, Vorst O (2002) DNA microarrays for functional plant genomics. Plant Mol Biol 48:99–118

    Article  PubMed  CAS  Google Scholar 

  • Allen JO (2005) Effect of teosinte cytoplasmic genomes on maize phenotype. Genetics 169:863–880

    Article  PubMed  CAS  Google Scholar 

  • Allen TD, Nuss DL (2004) Specific and common alterations in host gene transcript accumulation following infection of the chestnut blight fungus by mild and severe hypoviruses. J Virol 78:4145–4155

    Article  PubMed  CAS  Google Scholar 

  • Ancillo G, Gadea J, Forment J, Guerri J, Navarro L (2007) Class Prediction of closely related plant varieties using gene expression profiling. J Exp Bot 58:1927–1933

    Article  PubMed  CAS  Google Scholar 

  • Andersson SGE, Karlberg O, Canback B, Kurland CG (2003) On the origin of mitochondria: a genomics perspective. Philos Trans R Soc Lond B Biol Sci 358:165–177

    Article  PubMed  CAS  Google Scholar 

  • Atienza SG, Martin AC, Ramirez MC, Martin A, Ballesteros J (2007) Effects of Hordeum chilense cytoplasm on agronomic traits in common wheat. Plant Breed 126:5–8

    Article  CAS  Google Scholar 

  • Babiychuk E, Schantz R, Cherep N, Weil JH, Gleba Y, Kushnir S (1995) Alterations in chlorophyll a/b binding proteins in Solanaceae cybrids. Mol Gen Genet 249:648–654

    Article  PubMed  CAS  Google Scholar 

  • Banga SS, Labana KS, Medhi BN (1984) Alternaria incidence in some alloplasmic lines of Indian mustard (Brassica juncea (L.) Coss.). Theor Appl Genet 67:195–196

    Article  Google Scholar 

  • Bassene J-B, Berti L, Carcouet E, Dhuique-Mayer C, Fanciullino A-L, Bouffin J, Ollitrault P, Froelicher Y (2008) Influence of mitochondria origin on fruit quality in a Citrus cybrid. J Agric Food Chem 56:8635–8640

    Article  PubMed  CAS  Google Scholar 

  • Bogdanova VS (2007) Inheritance of organelle DNA markers in a pea cross associated with nuclear–cytoplasmic incompatibility. Theor Appl Genet 114:333–339

    Article  PubMed  CAS  Google Scholar 

  • Butow RA, Avadhani NG (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14:1–15

    Article  PubMed  CAS  Google Scholar 

  • Cabasson CM, Luro F, Ollitrault P, Grosser JW (2001) Non-random inheritance of mitochondrial genomes in Citrus hybrids produced by protoplast fusion. Plant Cell Rep 20:604–609

    CAS  Google Scholar 

  • Cai X, Fu J, Deng X, Guo W (2007) Production and molecular characterization of potential seedless cybrid plants between pollen sterile Satsuma mandarin and two seedy Citrus cultivars. Plant Cell Tissue Organ Cult 90:275–283

    Article  Google Scholar 

  • Cai X, Fu J, Chen C, Guo W (2009) Cybrid/hybrid plants regenerated from somatic fusions between male sterile Satsuma mandarin and seedy tangelos. Sci Hortic 122:323–327

    Article  CAS  Google Scholar 

  • Carlsson J, Lagercrantz U, Sundstrorm J, Teixeira R, Wellmer F, Meyerowitz EM, Glimelius K (2007) Microarray analysis reveals altered expression of a large number of nuclear genes in developing cytoplasmic male sterile Brassica napus flowers. Plant J 49:452–462

    Article  PubMed  CAS  Google Scholar 

  • Carlsson J, Leino M, Sohlberg J, Sundstroem JF, Glimelius K (2008) Mitochondrial regulation of flower development. Mitochondrion 8:74–86

    Article  PubMed  CAS  Google Scholar 

  • Cholon A, Giaccia AJ, Lewis AD, Hickson I, Brown JM (1992) What role do glutathione S-transferases play in the cellular response to ionizing radiation? Int J Radiat Oncol Biol Phys 22:759–763

    Article  PubMed  CAS  Google Scholar 

  • Conesa A, Gotz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2go: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  PubMed  CAS  Google Scholar 

  • Dutilleul C, Garmier M, Noctor G, Mathieu C, Chetrit P, Foyer CH, Paepe Rd (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212–1226

    Article  PubMed  CAS  Google Scholar 

  • Fanciullino AL, Gancel AL, Froelicher Y, Luro F, Ollitrault P, Brillouet JM (2005) Effects of nucleo–cytoplasmic interactions on leaf volatile compounds from citrus somatic diploid hybrids. J Agric Food Chem 53:4517–4523

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  CAS  Google Scholar 

  • Grosser JW, Gmitter FG Jr, Tusa N, Recupero GR, Cucinotta P (1996) Further evidence of a cybridization requirement for plant regeneration from citrus leaf protoplasts following somatic fusion. Plant Cell Rep 15:672–676

    Article  CAS  Google Scholar 

  • Grosser JW, Ollitrault P, Olivares-Fuster O (2000) Somatic hybridization in citrus: an effective tool to facilitate variety improvement. In Vitro Cell Dev Biol Plant 36:434–449

    Article  Google Scholar 

  • Guo WW, Cai XD, Grosser JW (2004) Somatic cell cybrids and hybrids in plant improvement. In: Daniell H, Chase CD (eds) Molecular biology and biotechnology of plant organelles. Kluwer, Dordrecht, pp 635–659

    Chapter  Google Scholar 

  • Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25:461–486

    Article  PubMed  CAS  Google Scholar 

  • Kang J, Zhang G, Bonnema G, Fang Z, Wang X (2008) Global analysis of gene expression in flower buds of Ms-cd1 Brassica oleracea conferring male sterility by using an Arabidopsis microarray. Plant Mol Biol 66:177–192

    Article  PubMed  CAS  Google Scholar 

  • Kato M, Jodo S, Tanaka T (1990) Effect of Abyssinian mustard cytoplasm on CC genome of Brassica. Jpn J Breed 40:475–484

    CAS  Google Scholar 

  • Leino M, Teixeira R, Landgren M, Glimelius K (2003) Brassica napus lines with rearranged Arabidopsis mitochondria display CMS and a range of developmental aberrations. Theor Appl Genet 106:1156–1163

    PubMed  CAS  Google Scholar 

  • Liu Z, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40:159–185

    Article  PubMed  CAS  Google Scholar 

  • Lopez C, Soto M, Restrepo S, Piegu B, Cooke R, Delseny M, Tohme J, Verdier V (2005) Gene expression profile in response to Xanthomonas axonopodis pv. manihotis infection in cassava using a cDNA microarray. Plant Mol Biol 57:393–410

    Article  PubMed  CAS  Google Scholar 

  • Lossl A, Gotz M, Braun A, Wenzel G (2000) Molecular markers for cytoplasm in potato: male sterility and contribution of different plastid-mitochondrial configurations to starch production. Euphytica 116:221–230

    Article  CAS  Google Scholar 

  • Martinez-Godoy MA, Mauri N, Juarez J, Marques MC, Santiago J, Forment J, Gadea J (2008) A genome-wide 20K citrus microarray for gene expression analysis. BMC Genomics 9:318

    Article  PubMed  Google Scholar 

  • Matsuo M, Obokata J (2006) Remote control of photosynthetic genes by the mitochondrial respiratory chain. Plant J 47:873–882

    Article  PubMed  CAS  Google Scholar 

  • Mehta R, Chandler-Brown D, Ramos FJ, Shamieh LS, Kaeberlein M (2010) Regulation of mRNA translation as a conserved mechanism of longevity control. In: Tavernarakis N (ed) Protein metabolism and homeostasis in aging. Springer, Berlin, pp 14–29

    Chapter  Google Scholar 

  • Moreira CD, Chase CD, Gmitter FG Jr, Grosser JW (2000) Inheritance of organelle genomes in citrus somatic cybrids. Mol Breed 6:401–405

    Article  CAS  Google Scholar 

  • Moriguchi T, Hidaka T, Omura M, Motomura T, Akihama T (1996) Genotype and parental combination influence efficiency of cybrid induction in Citrus by electrofusion. Am Soc Hortic Sci 31:275–278

    Google Scholar 

  • Moriguchi T, Motomura T, Hidaka T, Akihama T, Omura M (1997) Analysis of mitochondrial genomes among Citrus plants produced by the interspecific somatic fusion of `Seminole’ tangelo with rough lemon. Plant Cell Rep 16:397–400

    CAS  Google Scholar 

  • Newton KJ, Coe EH Jr (1986) Mitochondrial DNA changes in abnormal growth (nonchromosomal stripe) mutants of maize. Proc Natl Acad Sci 83:7363–7366

    Article  PubMed  CAS  Google Scholar 

  • Newton KJ, Gabay-Laughnan S, De Paepe R (2004) Mitochondrial mutations in plants. In: Day DA, Millar AH, Whelan J (eds) Plant mitochondria: from genome to function. Kluwer, Dordrecht, pp 121–141

    Google Scholar 

  • Ollitrault P, Dambier D, Luro F (1996) Somatic hybridization in Citrus: some new hybrids and alloplasmic plants. Proc Int Soc Citricult 2:907–912

    Google Scholar 

  • Ollitrault P, Dambier D, Froelicher Y, Carreel F, d`Hont A, Luro F, Bruyere S, Cabasson C, Lotfy S, Joumaa A, Vanel F, Maddi F, Treanton K, Grisoni M (2000) Somatic hybridisation potential for Citrus germplasm utilization. Cah Agric 9:223–236

    Google Scholar 

  • Pelletier G, Budar F (2007) The molecular biology of cytoplasmically inherited male sterility and prospects for its engineering. Curr Opin Biotechnol 18:121–125

    Article  PubMed  CAS  Google Scholar 

  • Prakash S, Ahuja I, Upreti HC, Kumar VD, Bhat SR, Kirti PB, Chopra VL (2001) Expression of male sterility in alloplasmic Brassica juncea with Erucastrum canariense cytoplasm and the development of a fertility restoration system. Plant Breed 120:479–482

    Article  Google Scholar 

  • Priault P, Fresneau C, Noctor G, Paepe Rd, Cornic G, Streb P (2006) The mitochondrial CMSII mutation of Nicotiana sylvestris impairs adjustment of photosynthetic carbon assimilation to higher growth irradiance. J Exp Bot 57:2075–2085

    Article  PubMed  CAS  Google Scholar 

  • Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8:546–553

    Article  PubMed  CAS  Google Scholar 

  • Randolph JB, Waggoner AS (1997) Stability, specificity and fluorescence brightness of multiply-labeled fluorescent DNA probes. Nucleic Acids Res 25:2923–2929

    Article  PubMed  CAS  Google Scholar 

  • Rattan SIS (2010) Synthesis, modification and turnover of proteins during aging. In: Tavernarakis N (ed) Protein metabolism and homeostasis in aging. Springer, Berlin, pp 1–13

    Chapter  Google Scholar 

  • Reuzeau C, Cavalie G (1997) Changes in RNA and protein metabolism associated with alterations in the germination efficiency of sunflower seeds. Ann Bot 80:131–137

    Article  CAS  Google Scholar 

  • Rhoads DM, Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7:177–194

    Article  PubMed  CAS  Google Scholar 

  • Richly E, Leister D (2004) An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329:11–16

    Article  PubMed  CAS  Google Scholar 

  • Rost TL, Van’t Hof J (1973) Radiosensitivity, RNA, and protein metabolism of “Leaky” and arrested cells in sunflower root meristems (Helianthus annuus). Am J Bot 60:172–181

    Article  CAS  Google Scholar 

  • Sabar M, De Paepe R, Kouchkovsky Y (2000) Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol 124:1239–1250

    Article  PubMed  CAS  Google Scholar 

  • Sahi C, Singh A, Blumwald E, Grover A (2006) Beyond osmolytes and transporters: novel plant salt-stress tolerance-related genes from transcriptional profiling data. Physiol Plant 127:1–9

    Article  CAS  Google Scholar 

  • Saito W, Ohgawara T, Shimizu J, Ishii S, Kobayashi S (1993) Citrus cybrid regeneration following cell fusion between nucellar cells and mesophyll cells. Plant Sci 88:195–201

    Article  CAS  Google Scholar 

  • Thimm O, Auml Bl, Sing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  PubMed  CAS  Google Scholar 

  • Tusa N, Bosco SFD, Nigro F, Ippolito A (2000) Response of cybrids and a somatic hybrid of lemon to Phoma tracheiphila infections. HortScience 35:125–127

    Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci 98:5116–5121

    Article  PubMed  CAS  Google Scholar 

  • Uprety DC, Tomar VK (1993) Photosynthesis and drought resistance of Brassica carinata and its parent species. Photosynthetica 29:321–327

    Google Scholar 

  • Verma DPS, Marcus A (1973) Regulation of RNA synthesis in plant cell culture: delayed synthesis of ribosomal RNA during transition from the stationary phase to active growth. Dev Biol 30:104–114

    Article  PubMed  CAS  Google Scholar 

  • Voluevich EA, Buloichik AA (1992) Nucleocytoplasmic interactions in the resistance of wheat to fungal pathogens V Quantitative seedling resistance to powdery mildew in alloplasmic lines of the variety Penjamo 62. Genetika (Moskva) 28:82–88

    Google Scholar 

  • Wang L, Pan Z-Y, Guo W-W (2010) Proteomic analysis of leaves from a diploid cybrid produced by protoplast fusion between Satsuma mandarin and pummelo. Plant Cell Tissue Organ Cult. doi:10.1007/s11240-010-9764-y

  • Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    Article  PubMed  CAS  Google Scholar 

  • Xu XY, Liu JH, Deng XX (2006) Isolation of cytoplasts from Satsuma mandarin (Citrus unshiu Marc.) and production of alloplasmic hybrid calluses via cytoplast-protoplast fusion. Plant Cell Rep 25:533–539

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto M, Kobayashi S (1995) A cybrid plant produced by electrofusion between Citrus unshiu (satsuma mandarin) and C. sinensis (sweet orange). Plant Tissue Cult Lett 12:131–137

    CAS  Google Scholar 

  • Yamamoto M, Matsumoto R, Okudai N, Yamada Y (1997) Aborted anthers of Citrus result from gene-cytoplasmic male sterility. Sci Hortic 70:9–14

    Article  Google Scholar 

  • Yu JP, Nickels R, McIntosh L (2001) A genome approach to mitochondrial-nuclear communication in Arabidopsis. Plant Physiol Biochem 39:345–353

    Article  CAS  Google Scholar 

  • Zhu JH, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295

    Article  PubMed  CAS  Google Scholar 

  • Zubko MK (2004) Mitochondrial tuning fork in nuclear homeotic functions. Trends Plant Sci 9:61–64

    Article  PubMed  CAS  Google Scholar 

  • Zubko MK, Zubko EI, Ruban AV, Adler K, Mock HP, Misera S, Gleba YY, Grimm B (2001) Extensive developmental and metabolic alterations in cybrids Nicotiana tabacum (+Hyoscyamus niger) are caused by complex nucleo-cytoplasmic incompatibility. Plant J 25:627–639

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was subsided by the Collectivité Territoriale de Corse, the ‘Triploid mandarin breeding project (Proyectos de Investigación Fundamental no orientada; AGL 2008-00596) and the ‘Biotechnologia de citricos’ project (Prometeo 2008/12). GA gratefully acknowledge Conselleria de Agricultura, Pesca y Alimentación (Generalitat Valenciana) her contract (under Proy_IVIA09/03).

Author information

Authors and Affiliations

  1. Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UPR amélioration génétique des espèces à multiplication végétative, Avenue Agropolis-TA A-75/02, 34398, Montpellier Cedex 5, France

    Jean-Baptiste Bassene, Yann Froelicher & Patrick Ollitrault

  2. Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Proteccion Vegetal y Biotecnología, Ctra. Moncada-Náquera Km 5, 46113, Moncada, Valencia, Spain

    Luis Navarro, Patrick Ollitrault & Gema Ancillo

Authors
  1. Jean-Baptiste Bassene
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yann Froelicher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrick Ollitrault
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gema Ancillo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gema Ancillo.

Additional information

Communicated by R. Rose.

Electronic supplementary material

Below is the link to the electronic supplementary material.

299_2011_1014_MOESM1_ESM.xls

Table 1 (additional file). Genes with significant expression changes in the cybrid leaves compared to Eureka lemon (XLS 249 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bassene, JB., Froelicher, Y., Navarro, L. et al. Influence of mitochondria on gene expression in a citrus cybrid. Plant Cell Rep 30, 1077–1085 (2011). https://doi.org/10.1007/s00299-011-1014-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1014-1

Keywords

Search

Navigation