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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
Article

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.

Keywords

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

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

Notes

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 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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© 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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