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Proteomic Analysis of Pea (Pisum sativum L.) Response During Compatible and Incompatible Interactions with the Pea Aphid (Acyrthosiphon pisum H.)

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Abstract

Acyrthosiphon pisum (pea aphid) is considered to be one of the most agronomically damaging pests on pea and alfalfa crops, and is responsible for significant yield losses in agriculture. For the efficient control of the parasite, a better understanding of its interaction and associated resistance mechanisms at the molecular level is required. We used two-dimensional gel electrophoresis (2DE) coupled to mass spectrometry (MSMS) analysis to compare the leaf proteome of two pea accessions displaying different phenotypes to A. pisum infestation. Multivariate statistical analysis identified 203 differential proteins under the experimental conditions, 81 of which were identified using a combination of peptide mass fingerprinting (PMF) and MSMS fragmentation. Most of the identified proteins corresponded to amino acid and carbohydrate metabolism, photosynthesis, folding/degradation, stress response, signal transduction and transcription/translation. Results suggested the involvement of different metabolic pathways that may be activated in order to overcome pea aphid attack in the resistant accession (P665): reduction of photosynthesis and amino acid biosynthesis that may be helpful in tackling pea aphid attack by limiting access to nutrients, up-accumulation of wound signal molecules such as LOXs and LAPs, and activation of the antioxidant ASC-GSH cycle. In contrast, the susceptible accession (cv. Messire) showed an increase in primary metabolism pathways (especially amino acid biosynthesis), from which a relationship to the successful performance of aphids on this accession could be inferred. Results are also discussed with regard to differences in management of photoassimilates against the strong sinks produced by aphid feeding.

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Abbreviations

ANOVA:

Analysis of variance

APX:

Ascorbate peroxidase

ASC-GSH:

Ascorbate-Glutathione cycle

BLAST:

Basic local alignment search tool

CHAPS:

3-(3-cholamidopropyl) dimethylammonio-1propane sulfonate

DTT:

Dithiothreitol

EF-Tu:

Elongation factor Tu

FDR:

False discovery rate

GRPs:

Glycine rich-RNA binding proteins

IEF:

Isoelectric focusing

IPG:

Immobilized pH gradient

JA:

Jasmonic acid

LAPs:

Leucine Aminopeptidases

LOXs:

Lipoxygenases

MALDI-TOF:

Matrix-Assisted Laser Desorption/Ionization Time-of-Flight

MS:

Mass spectrometry

NCBI:

National Center for Biotechnology Information

PCA:

Principal component analysis

PMF:

Peptide mass fingerprinting

ROS:

Reactive oxygen species

SDS:

Sodium dodecyl sulphate

TCA:

Trichloroacetic acid

TFA:

Trifluoracetic acid

TF:

Transcription factor

2-DE:

Two-dimensional electrophoresis

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Acknowledgments

This research was supported by the Spanish AGL2011-22524 project. The authors would like to thank the research group of Dr. Pr. Singh (CSIRO, Australia) for their support and training with the pea aphid. E. Carrillo was funded by a grant from Cabildo de La Palma- CSIC PhD and Mª Angeles Castillejo by a postdoctoral fellowship from the Spanish Ministry of Education, through the Mobility Program R-D + I 2008–2011.

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Authors and Affiliations

  1. Institute for Sustainable Agriculture, CSIC, 4084, 14080, Córdoba, Spain

    E. Carrillo & D. Rubiales

  2. Department of Molecular Systems Biology, University of Vienna, 1090, Vienna, Austria

    M. A. Castillejo

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  1. E. Carrillo
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  2. D. Rubiales
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  3. M. A. Castillejo
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Correspondence to M. A. Castillejo.

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Table S1

Dataset containing protein expression intensity values for 411 protein spots selected due to prospective differential expression behavior. The expression values were obtained after data normalization using the PD-QuestTM Advanced 2D analysis software. Values are mean ± SD of three biological replicates. (DOCX 333 kb)

Table S2

PCA analysis at 24 hai and 84 hai. This analysis allows for generation of associations between proteins and experimental conditions. Protein spots are listed from highest to lowest log changes. (DOC 2285 kb)

Table S3

Fragmented peptides sequences obtained by MSMS analysis. (DOC 2433 kb)

Figure S1

Venn diagrams of the quantitative (a-d), and qualitative (e-h) changes in proteins between non-infested (a, e) and infested (b, f) accessions, as well as in response to the infestation in the susceptible Messire (c, g) and in the resistant P665 (d, h) accessions. M (Messire), P (P665), C (Control, non-infested), I (Infested), 24 (24 hai), 84 (84 hai). (PPTX 528 kb)

Figure S2

Mean log abundance intensities for protein spots identified by PCA and pairwise comparisons separately shown by sampling time (24 hai, 84 hai). (PC1+) protein spots positively correlated with PC1. (PC1-) protein spots negatively correlated with PC1. (PC2+) protein spots positively correlated with PC2. (PC2-) protein spots negatively correlated with PC2. (PC3+) protein spots positively correlated with PC3. (PC3-) protein spots negatively correlated with PC3. (a) Legend for graphs in panels. The mean log intensity values were calculated from the sample replications. (PPTX 1434 kb)

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Carrillo, E., Rubiales, D. & Castillejo, M.A. Proteomic Analysis of Pea (Pisum sativum L.) Response During Compatible and Incompatible Interactions with the Pea Aphid (Acyrthosiphon pisum H.). Plant Mol Biol Rep 32, 697–718 (2014). https://doi.org/10.1007/s11105-013-0677-x

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