Plant Molecular Biology

, Volume 101, Issue 1–2, pp 129–148 | Cite as

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

  • Fabio Valentinuzzi
  • Silvia Venuti
  • Youry Pii
  • Fabio Marroni
  • Stefano Cesco
  • Felix Hartmann
  • Tanja Mimmo
  • Michele Morgante
  • Roberto Pinton
  • Nicola TomasiEmail author
  • Laura Zanin


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.


Fe acquisition P acquisition RNA-seq Root exudates Root uptake Transcriptomic analyses 



1-Aminocyclopropane-1-carboxylate oxidase


AGAMOUS-like 42


Aluminum-activated malate transporter


APS reductase


ATP sulfurylase


Auxin-responsive proteins


Basic helix-loop-helix


Chalcone synthase


Chalcone synthase


Chorismate mutase


Dihydroflavonol 4-reductase


Ethylene response factor




Ferric reductase defective


Ferric reduction oxidase


Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase


HXXXD-type acyl-transferase


Iron transporter


Low phosphate root1


Multidrug and toxin efflux transporter


Multidrug resistance-associated protein


Myeloblastosis family of transcription factors


Nicotianamine synthase


Natural macrophage resistant protein


Oligopeptide transporter


Purple acid phosphatases


Pleiotropic drug resistance







PHT transporters

High-affinity phosphate transporters


Phospholipase A 2A


P-starvation induced transporter

TCA cycle

Tricarboxylic acid cycle


Vacuolar iron transporter


Zinc-finger protein



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 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.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Supplementary material

11103_2019_896_MOESM1_ESM.docx (968 kb)
Supplementary material 1 (DOCX 967 kb)
11103_2019_896_MOESM2_ESM.xlsx (1.3 mb)
Supplementary material 2 (XLSX 1302 kb)
11103_2019_896_MOESM3_ESM.xlsx (72 kb)
Supplementary material 3 (XLSX 71 kb)
11103_2019_896_MOESM4_ESM.xlsx (895 kb)
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)


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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Fabio Valentinuzzi
    • 1
  • Silvia Venuti
    • 2
  • Youry Pii
    • 1
  • Fabio Marroni
    • 2
  • Stefano Cesco
    • 1
  • Felix Hartmann
    • 1
  • Tanja Mimmo
    • 1
  • Michele Morgante
    • 2
  • Roberto Pinton
    • 2
  • Nicola Tomasi
    • 2
    Email author
  • Laura Zanin
    • 2
  1. 1.Faculty of Science and TechnologyFree University of BolzanoBolzanoItaly
  2. 2.Dipartimento di Scienze Agroambientali, Alimentari e AnimaliUniversity of UdineUdineItaly

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