Skip to main content
SpringerLink
Log in

Common and specific responses to iron and phosphorus deficiencies in roots of apple tree (Malus × domestica)

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Iron and phosphorus are abundant elements in soils but poorly available for plant nutrition. The availability of these two nutrients represents a major constraint for fruit tree cultivation such as apple (Malus × domestica) leading very often to a decrease of fruit productivity and quality worsening. Aim of this study was to characterize common and specific features of plant response to Fe and P deficiencies by ionomic, transcriptomic and exudation profiling of apple roots. Under P deficiency, the root release of oxalate and flavonoids increased. Genes encoding for transcription factors and transporters involved in the synthesis and release of root exudates were upregulated by P-deficient roots, as well as those directly related to P acquisition. In Fe-deficiency, plants showed an over-accumulation of P, Zn, Cu and Mn and induced the transcription of those genes involved in the mechanisms for the release of Fe-chelating compounds and Fe mobilization inside the plants. The intriguing modulation in roots of some transcription factors, might indicate that, in this condition, Fe homeostasis is regulated by a FIT-independent pathway. In the present work common and specific features of apple response to Fe and P deficiency has been reported. In particular, data indicate similar modulation of a. 230 genes, suggesting the occurrence of a crosstalk between the two nutritional responses involving the transcriptional regulation, shikimate pathway, and the root release of exudates.

Key Message

For the first time, physiological and transcriptomic response of apple plants to Fe and P deficiencies have been thoroughly characterized and compared. Ionomic and transcriptomic analyses on apple roots have been performed and the data have been implemented with the metabolic profiling of root exudates. Our results highlighted that a physiological and transcriptional link occurs between the responses to Fe and P deficiencies in apple tree roots, which may contribute to the efficient strategy to mobilize nutrients from the soil exhibited by this plant species. Data of the present work highlight that the response to both Fe and P starvation shares common features in the modulation of transcription factors, the shikimate pathway and in the release of root exudates. To the best of our knowledge, this evidence suggests for the first time the existence of a cross talk between Fe and P nutritional pathways in tree plants.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All RNA-seq expression data are available at the public functional genomics data repository Gene Expression Omnibus (https://www.ncbi.nlm.nih.gov/geo) under the series entry (GSE122554; link:https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?&acc=GSE122554).

Abbreviations

ACO:

1-Aminocyclopropane-1-carboxylate oxidase

AGL42:

AGAMOUS-like 42

ALMT:

Aluminum-activated malate transporter

APR:

APS reductase

APS:

ATP sulfurylase

Aux/IAAs:

Auxin-responsive proteins

bHLH:

Basic helix-loop-helix

CHS:

Chalcone synthase

CHS:

Chalcone synthase

CM:

Chorismate mutase

DFR:

Dihydroflavonol 4-reductase

ERF:

Ethylene response factor

FER:

Ferritin

FRD:

Ferric reductase defective

FRO:

Ferric reduction oxidase

HCT:

Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase

HXXXD-type AT:

HXXXD-type acyl-transferase

IRT:

Iron transporter

LPR1:

Low phosphate root1

MATE:

Multidrug and toxin efflux transporter

MRP:

Multidrug resistance-associated protein

MYBs:

Myeloblastosis family of transcription factors

NAS:

Nicotianamine synthase

NRAMP:

Natural macrophage resistant protein

OPT:

Oligopeptide transporter

PAP:

Purple acid phosphatases

PDR:

Pleiotropic drug resistance

PFK:

Phosphofructokinase

PFK:

Phosphofructokinase

PHO:

PHOSPHATE protein

PHT transporters:

High-affinity phosphate transporters

PLA2A:

Phospholipase A 2A

PS3:

P-starvation induced transporter

TCA cycle:

Tricarboxylic acid cycle

VIT:

Vacuolar iron transporter

ZFP:

Zinc-finger protein

References

  • Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles and fate of organic acids in soils: a review. South Afr J Bot 108:393–406

    Article  CAS  Google Scholar 

  • Ashburner M, Ball CA, Blake JA et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atanassova M, Georgieva S, Ivancheva K (2011) Total phenolic and total flavonoid contents, antioxidant capacity and biological contaminants in medicinal herbs. J Univ Chem Technol Metall 46:81–88

    CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Baldi E, Miotto A, Ceretta CA et al (2018) Soil-applied phosphorous is an effective tool to mitigate the toxicity of copper excess on grapevine grown in rhizobox. Sci Hortic 227:102–111

    Article  CAS  Google Scholar 

  • Baldwin JC, Karthikeyan AS, Raghothama KG (1999) LePS3, a novel phosphate starvation induced gene in tomato (abstract no. 937). Annual American Society of Plant Physiologists Meeting, July 24–28, Baltimore. American Society of Plant Physiologists, Rockville, MD, p 190

  • Baldwin JC, Karthikeyan AS, Raghothama KG (2001) LePS2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol 125:728–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barabote RD, Tamang DG, Abeywardena SN et al (2006) Extra domains in secondary transport carriers and channel proteins. Biochim Biophys Acta (BBA) Biomembr 1758:1557–1579

    Article  CAS  Google Scholar 

  • Bastiaanse H, Muhovski Y, Mingeot D, Lateur M (2015) Candidate defense genes as predictors of partial resistance in ‘Président Roulin’ against apple scab caused by Venturia inaequalis. Tree Genet Genomes 11:125

    Article  Google Scholar 

  • Bertin C, Yang X, Weston L (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Briat JF, Rouached H, Tissot N, Gaymardand F, Dubos C (2015) Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE1 (PHR1). Front Plant Sci 6:290

    Article  PubMed  PubMed Central  Google Scholar 

  • Brumbarova T, Matros A, Mock H-P, Bauer P (2008) A proteomic study showing differential regulation of stress, redox regulation and peroxidase proteins by iron supply and the transcription factor FER. Plant J 54:321–334

    Article  CAS  PubMed  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 329:1–25

    Article  CAS  Google Scholar 

  • Cesco S, Mimmo T, Tonon G et al (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149

    Article  CAS  Google Scholar 

  • Chiou T-J, Lin S-I (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206

    Article  CAS  PubMed  Google Scholar 

  • Chow CN, Zheng HQ, Wu NY, Chien CH, Huang HD, Lee TY et al (2015) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res 44:1154

    Article  CAS  Google Scholar 

  • Colangelo EP, Lou Guerinot M (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colombo C, Palumbo G, He J-Z, Pinton R, Cesco S (2013) Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J Soils Sediments 14:1–11

    Google Scholar 

  • Csog Á, Mihucz VG, Tatár E et al (2011) Accumulation and distribution of iron, cadmium, lead and nickel in cucumber plants grown in hydroponics containing two different chelated iron supplies. J Plant Physiol 168:1038–1044

    Article  CAS  PubMed  Google Scholar 

  • Cui Y, Chen CL, Cui M, Zhou WJ, Wu HL, Ling HQ (2018) Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in Arabidopsis. Mol Plant 11:1166–1183

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Mari S (2017) New routes for plant iron mining. New Phytol 214:521–525

    Article  CAS  PubMed  Google Scholar 

  • Curie C, Cassin G, Couch D et al (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11

    Article  CAS  PubMed  Google Scholar 

  • Daccord N, Celton JM, Linsmith G et al (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49:1099–1106

    Article  CAS  PubMed  Google Scholar 

  • Donnini S, Prinsi B, Negri AS, Vigani G, Espen L, Zocchi G (2010) Proteomic characterization of iron deficiency responses in Cucumis sativus L. roots. BMC Plant Biol 10(1):268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54:965–975

    Article  CAS  PubMed  Google Scholar 

  • Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatase in plant phosphorus metabolism. Physiol Plant 90:791–800

    Article  CAS  Google Scholar 

  • Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan F, Cui B, Zhang T, Qiao G, Ding G, Wen X (2014) The temporal transcriptomic response of Pinus massoniana seedlings to phosphorus deficiency. PLoS ONE 9:e105068

    Article  PubMed  PubMed Central  Google Scholar 

  • FAOSTAT (2013) Statistical database of the food and agricultural organization. Available online at http://faostat.fao.org/site/567/DesktopDefault.aspx%3FPageID=567%23ancor

  • Fourcroy P, Sisó-Terraza P, Sudre D et al (2014) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201:155–167

    Article  CAS  PubMed  Google Scholar 

  • Gerke J (2000) Mathematical modelling of iron uptake by Graminaceous species as affected by iron forms in soil and phytosiderophore efflux. J Plant Nutr 23:1579–1587

    Article  CAS  Google Scholar 

  • Gottardi S, Tomasi N, Pinton R et al. (2013) Characterisation of a genistein transporter in roots of Lupin plants. Proceedings book of the 17th international plant nutrition colloquium and boron satellite meeting, Sabanci University, Istanbul, Turkey, 19–22 Aug 2013, p 27–28

  • Gu M, Chen A, Sun S, Xu G (2016) Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: what is missing? Mol Plant 9:396–416

    Article  CAS  PubMed  Google Scholar 

  • Hamburger D, Rezzonico E, MacDonald-Comber Petetot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  • Hansen N, Hopkins BG, Ellsworth JW, Jolley VD (2006) Iron nutrition in field crops. In: Barton LL, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Dordrecht, pp 61–83

    Google Scholar 

  • Hirsch J, Marin E, Floriani M et al (2006) Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 88:1767–1771

    Article  CAS  PubMed  Google Scholar 

  • Jakoby M, Wang HY, Reidt W, Weisshaar B, Bauer P (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577:528–534

    Article  CAS  PubMed  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Kim SA, Punshon T, Lanzirotti A et al (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295–1298

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    Article  CAS  PubMed  Google Scholar 

  • Korshunova Y, Eide D, Clark WG, Guerinot ML, Pakrasi H (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44

    Article  CAS  PubMed  Google Scholar 

  • Lee T, Yang S, Kim E, Ko Y, Hwang S, Shin J et al (2015) AraNet v2: an improved database of co-functional gene networks for the study of Arabidopsis thaliana and 27 other nonmodel plant species. Nucleic Acids Res 43:D996–1002

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wu X-D, Hao S-T, Wang X-J, Ling H-Q (2008) Proteomic response to iron deficiency in tomato root. Proteomics 8:2299–2311

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Wang N, Zhao F et al (2014) Changes in the transcriptomic profiles of maize roots in response to iron-deficiency stress. Plant Mol Biol 85:349–363

    Article  CAS  PubMed  Google Scholar 

  • Licciardello C, Torrisi B, Allegra M et al (2013) A transcriptomic analysis of sensitive and tolerant citrus rootstocks under natural iron deficiency conditions. J Am Soc Hortic Sci 138:487–498

    Article  CAS  Google Scholar 

  • Lin SI, Chiang SF, Lin WY et al (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57:389–399

    Article  CAS  PubMed  Google Scholar 

  • Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22:2219–2236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Rayo S, Di Foggia M, Rodrigues Moreira E et al (2015) Physiological responses in roots of the grapevine rootstock 140 Ruggeri subjected to Fe deficiency and Fe-heme nutrition. Plant Physiol Biochem 96:171–179

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lucena C, Porras R, Romera FJ, Alcántara E, García MJ, Pérez-Vicente R (2018) Similarities and differences in the acquisition of Fe and P by dicot plants. Agronomy 8:148

    Article  Google Scholar 

  • Lv Q, Zhong Y, Wang Y et al (2014) SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. Plant Cell 26:1586–1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marschner H, Römheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9:695–713

    Article  CAS  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J 17:10–12

    Article  Google Scholar 

  • Mendoza-Cózatl DG, Xie Q, Akmakjian GZ et al (2014) OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Mol Plant 7:1455–1469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mimmo T, Del Buono D, Terzano R et al (2014) Rhizospheric organic compounds in the soil-microorganism-plant system: their role in iron availability. Eur J Soil Sci 65:629–642

    Article  CAS  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT et al (2008) In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Berlin, pp 339–365

    Chapter  Google Scholar 

  • Neumann G, Römheld V (2011) Rhizosphere chemistry in relation to plant nutrition. In Marschner’s mineral nutrition of higher plants. Academic Press, Massachusetts, pp 347–368

    Google Scholar 

  • Nussaume L, Kanno S, Javot H et al (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2:83

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Rourke JA, Nelson RT, Grant D et al (2009) Integrating microarray analysis and the soybean genome to understand the soybeans iron deficiency response. BMC Genom 10:376

    Article  CAS  Google Scholar 

  • O’Rourke JA, Yang SS, Miller SS et al (2013) An RNA-Seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 161:705–724

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36–e36

    Article  PubMed  PubMed Central  Google Scholar 

  • Pii Y, Cesco S, Mimmo T (2015) Shoot ionome to predict the synergism and antagonism between nutrients as affected by substrate and physiological status. Plant Physiol Biochem 94:48–56

    Article  CAS  PubMed  Google Scholar 

  • Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puga MI, Mateos I, Charukesi R et al (2014) SPX1 is a phosphate-dependent inhibitor of phosphate starvation response 1 in Arabidopsis. Proc Natl Acad Sci USA 111:14947–14952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693

    Article  CAS  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    Article  CAS  PubMed  Google Scholar 

  • Rellán-Álvarez R, Andaluz S, Rodríguez-Celma J et al (2010) Changes in the proteomic and metabolic profiles of Beta vulgaris root tips in response to iron deficiency and resupply. BMC Plant Biol 10:120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Celma J, Lattanzio G, Grusak MA, Abadía A, Abadía J, López-Millán A-F (2011) Root responses of Medicago truncatula plants grown in two different iron deficiency conditions: changes in root protein profile and riboflavin Biosynthesis. J Proteom Res 10:2590–2601

    Article  CAS  Google Scholar 

  • Rose TJ, Kretzschmar T, Liu L, Lancaster G, Wissuwa M (2016) Phosphorus deficiency alters nutrient accumulation patterns and grain nutritional quality in rice. Agronomy 6:52

    Article  Google Scholar 

  • Rouached H, Arpat AB, Poirier Y (2010) Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant 3:288–299

    Article  CAS  PubMed  Google Scholar 

  • Sandnes A, Eldhuset TD, Wollebæk G (2005) Organic acids in root exudates and soil solution of Norway spruce and silver birch. Soil Biol Biochem 37:259–269

    Article  CAS  Google Scholar 

  • Santos CS, Silva AI, Serrão I, Carvalho AL, Vasconcelos MW (2013) Transcriptomic analysis of iron deficiency related genes in the legumes. Food Res Int 54:1162–1171

    Article  CAS  Google Scholar 

  • Schachtman DP (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid NB, Giehl RFH, Döll S et al (2014) Feruloyl-CoA 6′-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiol 164:160–172

    Article  CAS  PubMed  Google Scholar 

  • Secco D, Wang C, Arpat BA et al (2012) The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol 193:842–851

    Article  CAS  PubMed  Google Scholar 

  • Secco D, Shou H, Whelan J, Berkowitz O (2014) RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin. BMC Genom 15:230

    Article  CAS  Google Scholar 

  • Sharma T, Dreyer I, Kochian L, Piñeros MA (2016) The ALMT family of organic acid transporters in plants and their involvement in detoxification and nutrient security. Front Plant Sci 7:1488

    PubMed  PubMed Central  Google Scholar 

  • Sivitz AB, Hermand V, Curie C, Vert G (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS ONE 7:e44843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang H, Li X, Zu C, Zhang F, Shen J (2013) Spatial distribution and expression of intracellular and extracellular acid phosphatases of cluster roots at different developmental stages in white lupin. J Plant Physiol 170:1243–1250

    Article  CAS  PubMed  Google Scholar 

  • Thimm O, Essigmann B, Kloska S, Altmann T, Buckhout TJ (2001) Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol 127:1030–1043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian T, Liu Y, Yan H et al (2017) AgriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45:W122–W129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomasi N, Mimmo T, Terzano R et al (2014) Nutrient accumulation in leaves of Fe-deficient cucumber plants treated with natural Fe complexes. Biol Fertil Soils 50:973–982

    Article  CAS  Google Scholar 

  • Trapnell C, Williams BA, Pertea G et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valentinuzzi F, Cesco S, Tomasi N, Mimmo T (2015a) Influence of different trap solutions on the determination of root exudates in Lupinus albus L. Biol Fertil Soils 51:1–9

    Article  CAS  Google Scholar 

  • Valentinuzzi F, Mason M, Scampicchio M, Andreotti C, Cesco S, Mimmo T (2015b) Enhancement of the bioactive compound content in strawberry fruits grown under iron and phosphorus deficiency. J Sci Food Agric 95:2088–2094

    Article  CAS  PubMed  Google Scholar 

  • Valentinuzzi F, Pii Y, Vigani G, Lehmann M, Cesco S, Mimmo T (2015c) Phosphorus and iron deficiencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria × ananassa. J Exp Bot 66:6483–6495

    Article  CAS  PubMed  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Venuti S, Zanin L, Marroni F et al (2019) Physiological and transcriptomic data highlight common features between iron and phosphorus acquisition mechanisms in white lupin roots. Plant Sci 285:110

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Cui Y, Liu Y et al (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6:503–513

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Lu B, Wu T et al (2014a) Transcriptomic analysis demonstrates the early responses of local ethylene and redox signaling to low iron stress in Malus xiaojinensis. Tree Genet Genomes 10:573–584

    Article  Google Scholar 

  • Wang Z, Straub D, Yang H et al (2014b) The regulatory network of cluster-root function and development in phosphate-deficient white lupin (Lupinus albus) identified by transcriptome sequencing. Physiol Plant 151:323–338

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Ruan W, Shi J et al (2014c) Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci USA 111:14953–14958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters BM, McInturf SA, Amundsen K (2014) Transcriptomic and physiological characterization of the fefe mutant of melon (Cucumis melo) reveals new aspects of iron-copper crosstalk. New Phytol 203:1128–1145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu P, Ma L, Hou X et al (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260–1271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong H, Kakei Y, Kobayashi T et al (2013) Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil. Plant Cell Environ 36:1888–1902

    Article  CAS  Google Scholar 

  • Yang XJ, Finnegan PM (2010) Regulation of phosphate starvation responses in higher plants. Ann Bot 105:513–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Wu H, Wang N et al (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397

    Article  CAS  PubMed  Google Scholar 

  • Zamboni A, Zanin L, Tomasi N et al (2012) Genome-wide microarray analysis of tomato roots showed defined responses to iron deficiency. BMC Genom 13:101

    Article  CAS  Google Scholar 

  • Zancan S, Cesco S, Ghisi R (2006) Effect of UV-B radiation on iron content and distribution in maize plants. Environ Exp Bot 55:266–272

    Article  CAS  Google Scholar 

  • Zanin L, Tomasi N, Rizzardo C et al (2015) Iron allocation in leaves of Fe-deficient cucumber plants fed with natural Fe complexes. Physiol Plant 154:82–94

    Article  CAS  PubMed  Google Scholar 

  • Zanin L, Venuti S, Tomasi N (2016) Short-term treatment with the urease inhibitor N-(n-butyl) thiophosphoric triamide (NBPT) alters urea assimilation and modulates transcriptional profiles of genes involved in primary and secondary metabolism in maize seedlings. Front Plant Sci 22:845

    Google Scholar 

  • Zanin L, Venuti S, Zamboni A, Varanini Z, Tomasi N, Pinton R (2017) Transcriptional and physiological analyses of Fe deficiency response in maize reveal the presence of Strategy I components and Fe/P interactions. BMC Genom 18:154

    Article  CAS  Google Scholar 

  • Zanin L, Venuti S, Marroni F, Franco A, Morgante M, Pinton R, Tomasi N (2019) Physiological and RNA sequencing data of white lupin plants grown under Fe and P deficiency. Data in Brief 25:104069

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng H, Wang G, Zhang Y et al (2015) Genome-wide identification of phosphate-deficiency-responsive genes in soybean roots by high-throughput sequencing. Plant Soil 398:207–227

    Article  CAS  Google Scholar 

  • Zhai Z, Gayomba SR, Jung HI et al (2014) OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. Plant Cell 26:2249–2264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J-H, Mao Z-Q, Wang L-Q, Shu H-R (2007) Bioassay and identification of root exudates of three fruit tree species. J Integr Plant Biol 49:257–261

    Article  CAS  Google Scholar 

  • Zhang F, Shen J, Zhang J, Zuo Y, Li L, Chen X (2010) Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China. Elsevier, Amsterdam

    Google Scholar 

  • Zheng L, Huang F, Narsai R et al (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151:262–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Research was supported by grants from Italian MIUR (FIRB-Programma “Futuro in Ricerca” RBFR127WJ9), Free University of Bolzano (TN5056). RNA sequencing analyses were performed at the Institute of Applied Genomics (IGA, Udine).

Author information

Author notes

  1. Fabio Valentinuzzi and Silvia Venuti have contributed equally to this work.

Authors and Affiliations

  1. Faculty of Science and Technology, Free University of Bolzano, Piazza Università 5, 39100, Bolzano, Italy

    Fabio Valentinuzzi, Youry Pii, Stefano Cesco, Felix Hartmann & Tanja Mimmo

  2. Dipartimento di Scienze Agroambientali, Alimentari e Animali, University of Udine, via delle Scienze 206, 33100, Udine, Italy

    Silvia Venuti, Fabio Marroni, Michele Morgante, Roberto Pinton, Nicola Tomasi & Laura Zanin

Authors
  1. Fabio Valentinuzzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Silvia Venuti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Youry Pii
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabio Marroni
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stefano Cesco
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Felix Hartmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tanja Mimmo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michele Morgante
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Roberto Pinton
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nicola Tomasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Laura Zanin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FV, SV, YP, FH, LZ conducted experiments; FV, SV, SC, TM, RP, NT and LZ conceived and designed research; FV, SV, YP, FM, MM and LZ analysed -omic data. FV, YP, LZ, NT wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Nicola Tomasi.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 967 kb)

Supplementary material 2 (XLSX 1302 kb)

Supplementary material 3 (XLSX 71 kb)

11103_2019_896_MOESM4_ESM.xlsx

Table S9: Analyses of TFs-promoter binding sites of Arabidospis homologous to genes commonly modulated by by –Fe vs +P+Fe and –P vs +P+Fe (performed by PlantPAN 2.0, Chow et al., 2015) (XLSX 895 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valentinuzzi, F., Venuti, S., Pii, Y. et al. Common and specific responses to iron and phosphorus deficiencies in roots of apple tree (Malus × domestica). Plant Mol Biol 101, 129–148 (2019). https://doi.org/10.1007/s11103-019-00896-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00896-w

Keywords

Search

Navigation