Advertisement

Tree Genetics & Genomes

, 15:19 | Cite as

A transcriptional analysis reveals an extensive range of genes responsible for increasing the tolerance of Carrizo citrange to oxygen deficiency

  • Concetta LicciardelloEmail author
  • Paola Tononi
  • Marzia Rossato
  • Massimo Delledonne
  • Paola Caruso
Original Article
  • 144 Downloads
Part of the following topical collections:
  1. Gene Expression

Abstract

Little information is available on the Citrus genus and its relatives with regard to their ability to tolerate oxygen deficiency, establishing physiological and structural modifications. In order to gain insight into how citrus rootstocks respond to low-oxygen stress, a transcriptomic analysis (using a custom microarray) was performed on Carrizo citrange (CC) seedlings. These seedlings were transformed with OsMybleu transcription factor (TF), known for inducing tolerance to oxygen deficiency, and compared with CC wildtype. They were flushed for 24 h with N2 and microarray, carrying out expressed sequence tags of Citrus and relatives isolated from the roots, was hybridized with RNA of roots before and after hypoxia treatment. The genes involved in fermentation, Krebs cycle, sugar metabolism, cell wall metabolism, hormones, and TFs all resulted significantly altered in response to hypoxia in both samples. Quantitative expression analysis was performed on 42 selected genes to validate microarray results. The outcome was that most of them were confirmed. The main results lead to the conclusion that CC is naturally tolerant to oxygen limitation. Transformed CC responded to hypoxia by activating the main genes which are known in other plants to be responsible for this type of tolerance such as pyruvate decarboxylase and alcohol dehydrogenase. Among TFs, several were also induced, such as an HDZipIII homologous to AtHB15, target of mir166, itself overexpressed exclusively in transformed CC under hypoxia compared with all other samples. The present manuscript represents one of the very few investigative works focused on hypoxia-responsive transcriptional networks in citrus.

Keywords

Citrus Hypoxia Expression analysis miRNA Transcription factors 

Notes

Acknowledgements

The authors would like to thank Giuseppina Las Casas for assisting in the final analysis of the qRT-PCR.

Author contribution statement

CL wrote the article, performed the array hybridization and qRT-PCR validation, PT and MZ analyzed array data, MD supported in the array data, and PC provided research idea and contributed in the writing of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

Microarray expression data are available at NCBI GEO database (Edgar et al. 2002) with GEO number GSE86208.

Supplementary material

11295_2019_1327_MOESM1_ESM.docx (113 kb)
ESM 1 (DOCX 113 kb)

References

  1. Abts W, Vandenbussche B, De Proft MP, Van de Poel B (2017) The role of auxin-ethylene crosstalk in orchestrating primary root elongation in sugar beet. Front Plant Sci 8:444.  https://doi.org/10.3389/fpls.2017.00444 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arbona V, Hossain Z, Lopez-Climent MF et al (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466PubMedGoogle Scholar
  3. Arbona V, Zandalinas SI, Manzi M, Gonzalez-Guzman M, Rodriguez PL, Gomez-Cadenas A (2017) Depletion of abscisic acid levels in roots of flooded Carrizo citrange (Poncirus trifoliata L. Raf. x Citrus sinensis L. Osb.) plants is a stress-specificresponse associated to the differential expression of PYR/PYL/RCARreceptors. Plant Mol Biol 93:623–640PubMedGoogle Scholar
  4. Argamasilla R, Gómez-Cadenas A, Arbona V (2014) Metabolic and Regulatory Responses in Citrus Rootstocks in Response to Adverse Environmental Conditions. J Plant Growth Regul 33:169–180Google Scholar
  5. Armstrong W, Drew MC (2002) Root growth and metabolism under oxygen deficiency. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, 3rd edn. Marcel Dekker, New York, pp 729–761Google Scholar
  6. Baima S, Forte V, Possenti M, Peñalosa A, Leoni G, Salvi S, Felici B, Ruberti I, Morelli G (2014) Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module. Mol Plant 7:1006–1025PubMedGoogle Scholar
  7. Banti V, Giuntoli B, Gonzali S, Loreti E, Magneschi L, Novi G, Paparelli E, Parlanti S, Pucciariello C, Santaniello A, Perata P (2013) Low oxygen response mechanisms in green organisms. Int J Mol Sci 14:4734–4761PubMedPubMedCentralGoogle Scholar
  8. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:79–194Google Scholar
  9. Bradford KJ, Yang SF (1980) Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. Plant Physiol 65:322–326PubMedPubMedCentralGoogle Scholar
  10. Bradford KJ, Hsiao TC, Yang SF (1982) Inhibition of ethylene synthesis in tomato plants subjected to anaerobic root stress. Plant Physiol 70:1503–1507PubMedPubMedCentralGoogle Scholar
  11. Caruso P, Baldoni E, Mattana M et al (2011) Ectopic expression of a rice transcription factor, Mybleu, enhances tolerance of transgenic plants of Carrizo citrange to low oxygen stress. Plant Cell Tissue Organ Cult 109:327–339Google Scholar
  12. Chen X, Chen Z, Zhao H, Zhao Y, Cheng B, Xiang Y (2014) Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments. PLoS One 9:e87156.  https://doi.org/10.1371/journal.pone.0087156 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Choi WG, Roberts DM (2007) Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J Biol Chem 282:24209–24218PubMedGoogle Scholar
  14. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39(Web Server issue):W155–W159PubMedPubMedCentralGoogle Scholar
  15. Dennis ES, Dolferus R, Ellis M, Rahman M, Wu Y, Hoeren FU, Grover A, Ismond KP, Good AG, Peacock WJ (2000) Molecular strategies for improving waterlogging tolerance in plants. J Exp Bot 51:89–97PubMedGoogle Scholar
  16. Devi MJ, Taliercio EW, Sinclair TR (2015) Leaf expansion of soybean subjected to high and low atmospheric vapour pressure deficits. J Exp Bot 66(7):1845–1850PubMedPubMedCentralGoogle Scholar
  17. Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250PubMedGoogle Scholar
  18. Duong S, Vonapartis E, Li C-Y, Patel S, Gazzarrini S (2017) The E3 ligase ABI3-INTERACTING PROTEIN2 negatively regulates FUSCA3 and plays a role in cotyledon development in Arabidopsis thaliana. J Exp Bot 68:1555–1567PubMedPubMedCentralGoogle Scholar
  19. Edgar RM, Domrachevand W, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210PubMedPubMedCentralGoogle Scholar
  20. Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia – is survival a balancing act? Trends Plant Sci 9:449–456PubMedGoogle Scholar
  21. García-Sánchez F, Syvertsen JP, Gimeno V, Botía P, Perez-Perez JG (2007) Responses to flooding and drought stress by two citrus rootstock seedlings with different water-use efficiency. Physiol Plant 130:532–542Google Scholar
  22. Gasch P, Fundinger M, Müller JT et al (2016) Redundant ERF-VII transcription factors bind an evolutionarily-conserved cis-motif to regulate hypoxia-responsive gene expression in Arabidopsis. Plant Cell 28:160–168PubMedGoogle Scholar
  23. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedGoogle Scholar
  24. Girhepuje PV, Shinde GB (2011) Transgenic tomato plants expressing a wheat endochitinase gene demonstrate enhanced resistance to Fusarium oxysporum f. sp. lycopersici. Plant Cell Tissue Organ Cult 105:243–251Google Scholar
  25. Götz S, García-Gómez JM, Terol J et al (2008) A: high-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435PubMedPubMedCentralGoogle Scholar
  26. Griffiths-Jones S, Grocock Russell J, van Dongen S et al (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34(Database issue):D140–D144PubMedGoogle Scholar
  27. Guerra-Guimarães L, Pinheiro C, Chaves I, Barros D, Ricardo C (2016) Protein dynamics in the plant extracellular space. Proteomes 4:22PubMedCentralGoogle Scholar
  28. Gupta KJ, Igamberdiev AU, Manjunatha G, Segu S, Moran JF, Neelawarne B, Bauwe H, Kaiser WM (2011) The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci 181:520–526PubMedGoogle Scholar
  29. Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R (2010) Arabidopsis RAP22: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol 153:757–772PubMedPubMedCentralGoogle Scholar
  30. Hossain Z, Lopez-Climent MF, Arbona V et al (2009) Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J Plant Physiol 166:1391–1404PubMedGoogle Scholar
  31. Hsu FC, Chou MY, Peng HP, Chou SJ, Shih MC (2011) Insights into hypoxic systemic responses based on analyses of transcriptional regulation in Arabidopsis. PLoS One 6:e28888PubMedPubMedCentralGoogle Scholar
  32. Hu Y, Vandenbussche F, Van Der Straeten D (2017) Regulation of seedling growth by ethylene and the ethylene–auxin crosstalk. Planta 245:467–489.  https://doi.org/10.1007/s00425-017-2651-6 CrossRefPubMedGoogle Scholar
  33. Huerta L, Forment J, Gadea J et al (2008) Gene expression analysis in citrus reveals the role of gibberellins on photosynthesis and stress. Plant Cell Environ 31:1620–1633PubMedGoogle Scholar
  34. Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol Plant 138:393–404PubMedGoogle Scholar
  35. Ismond Kathleen P, Dolferus R, De Pauw M et al (2003) Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway. Plant Physiol 132:1292–1302PubMedPubMedCentralGoogle Scholar
  36. Johnson JR, Cobb BG, Drew MC (1994) Hypoxic induction of anoxia tolerance in roots of ADH1 null Zea mays L. Plant Physiol 105:61–67PubMedPubMedCentralGoogle Scholar
  37. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53Google Scholar
  38. Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal K (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 13:544PubMedPubMedCentralGoogle Scholar
  39. Kennedy RA, Rumpho ME, Fox TC (1992) Anaerobic metabolism in plants. Plant Physiol 100:1–6PubMedPubMedCentralGoogle Scholar
  40. Kobe B, Kajava A (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725–732PubMedGoogle Scholar
  41. Kreuzwieser J, Katharine JH, Howell A et al (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473PubMedPubMedCentralGoogle Scholar
  42. Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231PubMedPubMedCentralGoogle Scholar
  43. Lee BK, Park MR, Srinivas B et al (2003) Induction of phenylalanine ammonia-lyase gene expression by paraquat and stress-related hormones in Rehmannia glutinosa. Mol Cell 16:34–39Google Scholar
  44. Li X, Xie X, Li J, Cui Y, Hou Y, Zhai L, Wang X, Fu Y, Liu R, Bian S (2017) Conservation and diversification of the miR166 family in soybean and potential roles of newly identified miR166s. BMC Plant Biol 17:32PubMedPubMedCentralGoogle Scholar
  45. Licausi F, Perata PD (2009) Low oxygen signaling and tolerance in plants. Adv Bot Res 50:139–198Google Scholar
  46. Licausi F, Weits DA, Pant BD, Scheible WR, Geigenberger P, van Dongen JT (2011) Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytol 190:442–456PubMedGoogle Scholar
  47. Licciardello C, Torrisi BF, Tononi P et al (2013) A transcriptomic analysis of sensitive and tolerant citrus rootstocks under natural iron deficiency conditions. J Am Soc Hortic Sci 138:487–498Google Scholar
  48. Liu F, VanToai T, Moy LP et al (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129PubMedPubMedCentralGoogle Scholar
  49. Liu H, Guo X, Naeem MS, Liu D, Xu L, Zhang W, Tang G, Zhou W (2011) Transgenic Brassica napus L. lines carrying a two genes construct demonstrate enhanced resistance against Plutella xylostella and Sclerotinia sclerotiorum. Plant Cell Tissue Organ Cult 106:143–151Google Scholar
  50. Loreti E, Poggi A, Novi G et al (2005) A genome-wide analysis of the effects of sucrose on gene expression in arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138PubMedPubMedCentralGoogle Scholar
  51. Magneschi L, Perata P (2009) Rice germination and seedling growth in the absence of oxygen. Ann Bot 103:181–196PubMedGoogle Scholar
  52. Mattana M, Vannini C, Espen L, Bracale M, Genga A, Marsoni M, Iriti M, Bonazza V, Romagnoli F, Baldoni E, Coraggio I, Locatelli F (2007) The rice Mybleu transcription factor increases tolerance to oxygen deprivation in Arabidopsis plants. Physiol Plant 131:106–121PubMedGoogle Scholar
  53. Mazzucotelli E, Belloni S, Marone D, de Leonardis A, Guerra D, di Fonzo N, Cattivelli L, Mastrangelo A (2006) The E3 ubiquitin ligase gene family in plants: regulation by degradation. Current Genomics 7:509–522PubMedPubMedCentralGoogle Scholar
  54. Meguro N, Tsuji H, Tsutsumi N et al (2006) Involvement of aldehyde dehydrogenase in alleviation of post-anoxic injury in rice. In: Rai AK, Takabe T (eds) Abiotic stress tolerance in plants: toward the improvement of global environment and food. Springer, The Netherlands, pp 111–119Google Scholar
  55. Mertens E, Larondelle Y, Hers HG (1990) Induction of pyrophosphate: fructose 6-phosphate 1-phosphotransferase by anoxia in rice seedlings. Plant Physiol 93:584–587PubMedPubMedCentralGoogle Scholar
  56. Mittler R, Vanderauwera S, Gollery M, van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedGoogle Scholar
  57. Mohanty B, Wilson PM, Rees T (1993) Effects of anoxia on growth and carbohydrate metabolism in suspension cultures of soybean and rice. Phytochem 34:75–82Google Scholar
  58. Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low oxygen stress highlights conserved and plant-specific responses. Plant Physiol 152:1484–1500PubMedPubMedCentralGoogle Scholar
  59. Nanjo Y, Maruyama K, Yasue H, Yamaguchi-Shinozaki K, Shinozaki K, Komatsu S (2011) Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Mol Biol 77:129–144PubMedGoogle Scholar
  60. Narsai R, Howell KA, Carroll A, Ivanova A, Millar AH, Whelan J (2009) Defining core metabolic and transcriptomic responses to oxygen availability in rice embryos and young seedlings. Plant Physiol 151:306–322PubMedPubMedCentralGoogle Scholar
  61. Ohashi-Ito K, Fukuda H (2003) HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44:1350–1358PubMedGoogle Scholar
  62. Oliveira TM, Silva FRD, Bonatto D et al (2015) Comparative study of the protein profiles of Sunki mandarin and Rangpur lime plants in response to water deficit. BMC Plant Biol 15(69):69PubMedPubMedCentralGoogle Scholar
  63. Ookawara R, Satoh S, Yoshioka T et al (2005) Expression of a-expansin and xyloglucan endotransglucosylase/hydrolase genes associated with shoot elongation enhanced by anoxia, ethylene and carbon dioxide in arrowhead (Sagittaria pygmaea Miq.) tubers. Ann Bot 96:693–702PubMedPubMedCentralGoogle Scholar
  64. Paytuvì GA, Hermoso PA, Martiınez de Lagran IA et al (2016) GREENC: a Wiki-based database of plant lncRNAs. Nuc Ac Res 44(Database issue):D1161–D1166Google Scholar
  65. Perazzolli M, Romero-Puertas MC, Delledonne M (2006) Modulation of nitric oxide bioactivity by plant haemoglobins. J Exp Bot 57:479–488PubMedGoogle Scholar
  66. Qi Y, Yamauchi Y, Ling J, Kawano N, Li D, Tanaka K (2005) The submergence-induced gene OsCTP in rice (Oryza sativa L.) is similar to Escherichia coli cation transport protein ChaC. Plant Sci 168:15–22Google Scholar
  67. Reddy PP (2014) Climate resilient agriculture for ensuring food security. Springer (Ed). doi: https://doi.org/10.1007/978-81-322-2199-9 Google Scholar
  68. Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626PubMedPubMedCentralGoogle Scholar
  69. Rudus I, Sasiak M, Kepczynski J (2013) Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-carboxylte oxidase (ACO) gene. Acta Physiol Plant 35:295–307Google Scholar
  70. Russell DA, Sachs MM (1991) The maize cytosolic glyceraldehyde-3-phosphate dehydrogenase gene family: organ-specific expression and genetic analysis. Mol Gen Genet 229:219–228PubMedGoogle Scholar
  71. Sairam RK, Dharmar K, Chinnusamy V, Meena RC (2009) Waterlogging-induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata). J Plant Physiol 166:602–616PubMedGoogle Scholar
  72. Schaffer B (2006) Effects of soil oxygen deficiency on avocado (Persea Americana Mill.) trees. Seminario International: Manejo del Riego y Suelo en el Cultivo del Palto La Cruz, Chile – 27 y 28 de SeptiembreGoogle Scholar
  73. Singh A, Roy S, Singh S, Das SS, Gautam V, Yadav S, Kumar A, Singh A, Samantha S, Sarkar AK (2017) Phytohormonal crosstalk modulates the expression of miR166/165s, target class III HDZIPs, and KANADI genes during root growth in Arabidopsis thaliana. Sci Rep 7:3408PubMedPubMedCentralGoogle Scholar
  74. Smith AM, Coupland G, Dolan L, Harberd N, Jones J, Martin C, Sablowski R, Amey A (2012) Gli stress ambientali. In: Zanichelli (ed.) Biologia delle piante, Vol. 2, 1st edn. Bologna, Italia, pp 49–100 ISBN 9788808129314Google Scholar
  75. Syvertsen J, Levy Y (2005) Salinity interactions with other abiotic and biotic stresses in citrus. HortTechnology 15:100–103Google Scholar
  76. Tanaka Y, Matsuoka M, Yamanoto N, Ohashi Y, Kano-Murakami Y, Ozeki Y (1989) Structure and characterization of a cDNA clone for phenylalanine ammonia-lyase from cut-injured roots of sweet potato. Plant Physiol 90:1403–1407PubMedPubMedCentralGoogle Scholar
  77. Van de Poe B, Van Der Straeten D (2014) 1-aminocyclopropane−1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front Plant Sci 5:640.  https://doi.org/10.3389/fpls.2014.00640 CrossRefGoogle Scholar
  78. Van Engelen FA, Hartog MV, Thomas TL et al (1993) The carrot secreted glycoprotein gene EP1 is expressed in the epidermis and has sequence homology to Brassica S-locus glycoproteins. Plant J 4(5):855–862PubMedGoogle Scholar
  79. Vandenbroucke K, Robbens S, Vandepoele K, Inze D, van de Peer Y, van Breusegem F (2008) Hydrogen peroxide-induced gene expression across kingdoms: a comparative analysis. Mol Biol Evol 25:507–516PubMedGoogle Scholar
  80. Vartapetian BB, Jackson MB (1997) Plant adaptations to anaerobic stress. Ann Bot 79(suppl 1):3–20Google Scholar
  81. Voesenek LCJ, Sasidharan R (2013) Ethylene--and oxygen signalling--drive plant survival during flooding. Plant Biol (Stuttg) 15:426–435Google Scholar
  82. Wang F, Deng XW (2011) Plant ubiquitin-proteasome pathway and its role in gibberellin signalling. Cell Res 21:1286–1294PubMedPubMedCentralGoogle Scholar
  83. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252Google Scholar
  84. Wu J, Zheng S, Feng G et al (2016) Comparative analysis of mirnas and their target transcripts between a spontaneous late-ripening sweet orange mutant and its wild-type using small RNA and degradome sequencing. Front Plant Sci 7:1416PubMedPubMedCentralGoogle Scholar
  85. Xia JH, Saglio PH (1992) Lactic acid efflux as a mechanism of hypoxic acclimation of maize root tips to anoxia. Plant Physiol 100:40–46PubMedPubMedCentralGoogle Scholar
  86. Xie ZX, Khanna K, Ruan SL (2012) Expression of microRNAs and its regulation in plants. Semin Cell Dev Biol 21:790–797Google Scholar
  87. Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25PubMedGoogle Scholar
  88. Yelenosky G, Vu JCV, Wutscher H (1995) Influence of paclobutrazol in the soil on growth, nutrient elements in the leaves, and flood/freeze tolerance of citrus rootstock seedlings. J Plant Growth Regul 14(3):129–134Google Scholar
  89. Zeng Y, Wu Y, Avigne WT, Koch KE (1999) Rapid repression of maize invertases by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiol 121:599–608PubMedPubMedCentralGoogle Scholar
  90. Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y (2008) Submergence-responsive MicroRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot 102:509–519PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.CREA, Research Centre for Olive, Citrus and Tree FruitAcirealeItaly
  2. 2.Dipartimento di BiotecnologieUniversità degli Studi di VeronaVeronaItaly

Personalised recommendations