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Class 1 non-symbiotic and class 3 truncated hemoglobin-like genes are differentially expressed in stone fruit rootstocks (Prunus L.) with different degrees of tolerance to root hypoxia

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Abstract

Root hypoxia produced by flooding or over-irrigation limits stone fruit tree development, particularly in orchards established on soils with restricted drainage. To overcome this problem, stone fruit trees are usually grafted on rootstocks (species or hybrid of the Prunus L. genus) with different degrees of tolerance to root hypoxia. However, the molecular base of such variability is largely unknown. In Arabidopsis thaliana (Heynh.), as well as in a number of crops and tree species, hemoglobin (Hb)-like genes stand out among hypoxia-related genes, but no such studies have been done with the Prunus species used as rootstocks. In this study, we analyzed the expression pattern of class 1 non-symbiotic Hb-like (nsHb) and class 3 truncated Hb-like (trHb) genes in Prunus rootstock roots with different responses to this stress. We observed that the putative Prunus nsHb and trHb genes were induced by root hypoxia in all analyzed Prunus genotypes, independently of their tolerance to hypoxia. However, Prunus nsHb and trHb genes had higher expression levels in roots of tolerant rootstocks. Prunus nsHb and trHb genes were also regulated by other abiotic stresses, such as salt stress and low temperatures. Our results suggest that changes in nsHb and trHb expressions could be part of the adaptive mechanisms that have evolved in the Prunus species to survive under hypoxia or other types of environmental stress that commonly challenge stone fruit tree orchards.

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References

  • Amador ML, Sancho S, Rubio-Cabetas MJ (2009) Biochemical and molecular aspects involved in waterlogging tolerance in Prunus rootstocks. Acta Hort 814:715–720

    CAS  Google Scholar 

  • Amador ML, Sancho S, Bielsa B, Gomez-Aparisi J, Rubio-Cabetas MJ (2012) Physiological and biochemical parameters controlling waterlogging stress tolerance in Prunus before and after drainage. Physiol Plant 144:657–668. doi:10.1111/j.1399–3054.2012.01568

    Article  Google Scholar 

  • Appleby CA (1992) The origin and functions of haemoglobin in plants. Sci Progr 76:365–398

    CAS  Google Scholar 

  • Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Ann Rev Plant Biol 59:313–339

    Article  CAS  Google Scholar 

  • Bustos-Sanmamed P, Tovar-Méndez A, Crespi M, Sato S, Tabata S, Becana M (2011) Regulation of nonsymbiotic and truncated hemoglobin genes of Lotus japonicus in plant organs and in response to nitric oxide and hormones. New Phytol 189:765–776

    Article  PubMed  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Christianson JA, Llewellyn DJ, Dennis ES, Wilson I (2010) Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.). Plant Cell Physiol 51:21–37

    Article  PubMed  CAS  Google Scholar 

  • Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611

    Article  PubMed  CAS  Google Scholar 

  • de Ollas C, Hernando B, Vicent Arbona V, Gómez-Cadenas A (2012) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147:296–306. doi:10.1111/j.1399-3054.2012.01659.x

    Article  PubMed  Google Scholar 

  • Dickerson RE, Geis I (1983) Hemoglobin: structure, function, evolution and pathology. Benjamin-Cummings, Menlo Park

    Google Scholar 

  • Domingo R, Pérez-Pastor A, Ruiz-Sánchez MC (2002) Physiological responses of apricot plants grafted on two different rootstocks to flooding conditions. J Plant Physiol 159:725–732

    Article  CAS  Google Scholar 

  • Dordas C (2009) Nonsymbiotic hemoglobins and stress tolerance in plants. Plant Sci 176:433–440

    Article  CAS  Google Scholar 

  • Garrocho-Villegas V, Bustos-Rivera G, Gough J, Vinogradov SN, Arredondo-Peter R (2008) Expression and in silico structural analysis of a rice (Oryza sativa) hemoglobin 5. Plant Physiol Biochem 46:855–859

    Article  PubMed  CAS  Google Scholar 

  • Gupta KJ, Igamberdiev AU (2011) The anoxic plant mitochondrion as nitrite: NO reductase. Mitochondrion 11:537–543

    Article  PubMed  CAS  Google Scholar 

  • Hill RD (2012) Non-symbiotic haemoglobins—what's happening beyond nitric oxide scavenging? AoB PLANTS: pls004. doi:10.1093/aobpla/pls004

    Google Scholar 

  • Horchani F, Philippe Gallusci P, Pierre Baldet P, Cabasson C, Maucourt M, Rolin D, Raymond P, Aschi-Smiti S (2008) Prolonged root hypoxia induces ammonium accumulation and decreases the nutritional quality of tomato fruits. J Plant Physiol 165:1352–1359

    Article  PubMed  CAS  Google Scholar 

  • Hunt PW, Klok EJ, Trevaskis B, Watts RA, Ellis MH, Peacock WJ, Dennis ES (2002) Increased level of hemoglobin 1 enhances survival of hypoxic stress and promotes early growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:17197–17202

    Article  PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Baron K, Manac'h-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Ann Bot 96:557–564

    Article  PubMed  CAS  Google Scholar 

  • Isaakidis A, Sotiropoulos T, Almaliotis D, Therios I, Stylianidis D (2004) Response to severe water stress of the almond (Prunus amygdalus) ‘Ferragnès’ grafted on eight rootstocks. New Zealand J Crop Hort Sci 32:355–362

    Article  Google Scholar 

  • Kennedy RA, Rumpho ME, Fox TC (1992) Anaerobic metabolism in plants. Plant Physiol 100:1–6

    Article  PubMed  CAS  Google Scholar 

  • Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiol Monog 1:1–29

    Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH et al (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  PubMed  CAS  Google Scholar 

  • Lira-Ruan V, Sarath G, Klucas RV, Arredondo-Peter R (2001) Synthesis of hemoglobins in rice (Oryza sativa var. Jackson) plants growing in normal and stress conditions. Plant Sci 161:279–287

    Article  PubMed  CAS  Google Scholar 

  • Mizutami F, Yamada M, Tomana T (1982) Differential water tolerance and ethanol accumulation in Prunus species under flooded conditions. J Jpn Soc Hort Sci 51:29–34

    Article  Google Scholar 

  • Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT (2011) Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol 190:472–487

    Article  PubMed  CAS  Google Scholar 

  • Nicolás E, Torrecillas A, Dell'Amico J, Alarcón JJ (2005) The effect of short-term flooding on the sap flow, gas exchange and hydraulic conductivity of young apricot trees. Trees 19:51–57

    Article  Google Scholar 

  • Niemann J, Tisa LS (2008) Nitric oxide and oxygen regulate truncated hemoglobin gene expression in Frankia strain CcI3. J Bacteriol 190:7864–7867

    Article  CAS  Google Scholar 

  • Ota M, Isogay Y, Nishikawa K (1997) Structural requirement of highly-conserved residues in globins. FEBS Lett 415:129–133

    Article  CAS  Google Scholar 

  • Parent C, Berger A, Folzer H, Dat J, Crevècoeur M, Badot PM, Capelli N (2008) A novel nonsymbiotic hemoglobin from oak: cellular and tissue specificity of gene expression. New Phytol 177(1):142–154

    PubMed  CAS  Google Scholar 

  • Parent C, Crèvecoeur M, Capelli N, Dat JF (2011) Contrasting growth and adaptive responses of two oak species to flooding stress: role of non-symbiotic haemoglobin. Plant Cell Environ 34:1113–1126

    Article  PubMed  CAS  Google Scholar 

  • Pinochet J (2010) Replantac (Rootpac R), a plum-almond hybrid rootstock for replant situations. HortSci 45:299–301

    Google Scholar 

  • Pistelli L, Iacona C, Miano D, Cirilli M, Colao MC, Mensuali-Sodi A, Muleo R (2012) Novel Prunus rootstock somaclonal variants with divergent ability to tolerate waterlogging. Tree Physiol 32(3):355–368

    Article  PubMed  CAS  Google Scholar 

  • Ranney TG (1994) Differential tolerance of eleven Prunus taxa to root zone flooding. J Environ Hortic 12:138–141

    Google Scholar 

  • Ranney TG, Bassuk NL, Withlow TH (1991) Influence of rootstock, scion, and water deficits on growth of Colt and Meteor cherry trees. HortSci 26:1204–1207

    Google Scholar 

  • Rubio-Cabetas MJ, Amador ML, Gómez-Aparisi J, Jaime J, Sancho S (2011) Physiological and biochemical parameters involved in waterlogging stress in Prunus. Acta Hort 903:1215–1224

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sánchez C, Cabrera JJ, Gates AJ, Bedmar EJ, Richardson DJ, Delgado MJ (2011) Nitric oxide detoxification in the rhizobia–legume symbiosis. Biochem Soc Trans 39:184–188

    Article  Google Scholar 

  • Sasakura F, Uchiumi T, Shimoda Y, Suzuki A, Takenouchi K, Higashi S, Abe M (2006) A class 1 hemoglobin gene from Alnus firma functions in symbiotic and nonsymbiotic tissues to detoxify nitric oxide. MPMI 19:441–450

    Article  PubMed  CAS  Google Scholar 

  • Sekse L (1995) Cuticular fracturing in fruits sweet cherry (Prunus avium L.) resulting from chancing soil water contents. J Hort Sci 70(4):631–635

    Google Scholar 

  • Sekse L (1998) Fruit cracking mechanism in sweet cherries (Prunus avium L.). Rev Acta Hort 468:637–648

    Google Scholar 

  • Shi X, Wang X, Peng F, Zhao Y (2012) Molecular cloning and characterization of a nonsymbiotic hemoglobin gene (GLB1) from Malus hupehensis Rehd. with heterologous expression in tomato. Mol Biol Rep 39:8075–8082. doi:10.10007/s11033-012-1654-4

    Article  PubMed  CAS  Google Scholar 

  • Shimoda Y, Nagata M, Suzuki A, Abe M, Sato S, Kato T, Tabata S, Higashi S, Uchiumi T (2005) Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol 46:99–107

    Article  PubMed  CAS  Google Scholar 

  • Sowa AW, Duff SMG, Guy PA, Hill RD (1998) Altering hemoglobin levels changes energy status in maize cells under hypoxia. Proc Natl Acad Sci USA 95:10317–10321

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Taylor ER, Nie XZ, MacGregor AW, Hill RD (1994) A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol Biol 24:853–862

    Article  PubMed  CAS  Google Scholar 

  • Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:71

    Article  PubMed  Google Scholar 

  • Trevaskis B, Watts RA, Andersson CR, Llewellyn DJ, Hargrove MS, Olson SO, Dennis ES, Peacock WJ (1997) Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc Natl Acad Sci USA 94:12230–12234

    Article  PubMed  CAS  Google Scholar 

  • Vázquez-Limón C, Hoogewijs D, Vinogradov SN, Arredondo-Peter R (2012) The evolution of land plant hemoglobins. Plant Sci 191–192:71–81

    Article  PubMed  Google Scholar 

  • Vieweg MF, Hohnjec N, Küster H (2005) Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220:757–766

    Article  PubMed  CAS  Google Scholar 

  • Vigeolas H, Hühn D, Geigenberger P (2011) Non-symbiotic hemoglobin-2 leads to an elevated energy state and to a combined increase in polyunsaturated fatty acids and total oil content when over-expressed in developing seeds of transgenic Arabidopsis plants. Plant Physiol 155:1435–1444

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Elhiti M, Hebelstrup KH, Hill RD, Stasolla C (2011) Manipulation of hemoglobin expression affects Arabidopsis shoot organogenesis. Plant Physiol Biochem 49:1108–1116

    Article  PubMed  CAS  Google Scholar 

  • Webster AD (2005) The origin, distribution and genetic diversity of temperate tree fruits. In: Tromp J, Webster AD, Wertheim SJ (eds) Fundamentals of temperate zone tree fruit production. Backhuys Publishers, Leiden, pp 1–11

    Google Scholar 

  • Wittenberg JB, Martino Bolognesi M, Beatrice A, Wittenberg BA, Michel Guertin M (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 277:871–874

    Article  PubMed  CAS  Google Scholar 

  • Zhao L, Riliang Gm Gao P, Wang G (2008) A nonsymbiotic hemoglobin gene from maize, ZmHb, is involved in response to submergence, high-salt and osmotic stresses. Plant Cell Tissue Organ Cult 95:227–237

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by grants from CONICYT Regional/CEAF/R08I1001 and FONDECYT Project 11110079. R.A. and P.P. were supported by grants from CONICYT (Project no. 79095006). M.J.A. was supported by CONICYT fellowships (AT-24100126 and 21080351). Rootstock plants were kindly provided by Agromillora Sur S.A.

Data archiving statement

The nucleotide sequences reported in this paper have been deposited in the GenBank database under the following accession numbers: JX966474 (Pc × Pm nsHb1), JX966475 (Pa nsHb1), and JX966476 (Pc × Pm trHb1).

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Correspondence to Rubén Almada.

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Communicated by D. Chagné

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Almada, R., Arismendi, M.J., Pimentel, P. et al. Class 1 non-symbiotic and class 3 truncated hemoglobin-like genes are differentially expressed in stone fruit rootstocks (Prunus L.) with different degrees of tolerance to root hypoxia. Tree Genetics & Genomes 9, 1051–1063 (2013). https://doi.org/10.1007/s11295-013-0618-8

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