Rootstock-regulated gene expression patterns associated with fire blight resistance in apple

Philip J. Jensen, Noemi Halbrendt, Gennaro Fazio, Izabela Makalowska, Naomi S. Altman, Craig Praul, Siela Maximova, Henry K. Ngugi, Robert Michael Crassweller, James W. Travis, Timothy W. McNellis

Research output: Contribution to journalArticle

43 Citations (Scopus)

Abstract

Background: Desirable apple varieties are clonally propagated by grafting vegetative scions onto rootstocks. Rootstocks influence many phenotypic traits of the scion, including resistance to pathogens such as Erwinia amylovora, which causes fire blight, the most serious bacterial disease of apple. The purpose of the present study was to quantify rootstock-mediated differences in scion fire blight susceptibility and to identify transcripts in the scion whose expression levels correlated with this response.Results: Rootstock influence on scion fire blight resistance was quantified by inoculating three-year old, orchard-grown apple trees, consisting of 'Gala' scions grafted to a range of rootstocks, with E. amylovora. Disease severity was measured by the extent of shoot necrosis over time. 'Gala' scions grafted to G.30 or MM.111 rootstocks showed the lowest rates of necrosis, while 'Gala' on M.27 and B.9 showed the highest rates of necrosis. 'Gala' scions on M.7, S.4 or M.9F56 had intermediate necrosis rates. Using an apple DNA microarray representing 55,230 unique transcripts, gene expression patterns were compared in healthy, un-inoculated, greenhouse-grown 'Gala' scions on the same series of rootstocks. We identified 690 transcripts whose steady-state expression levels correlated with the degree of fire blight susceptibility of the scion/rootstock combinations. Transcripts known to be differentially expressed during E. amylovora infection were disproportionately represented among these transcripts. A second-generation apple microarray representing 26,000 transcripts was developed and was used to test these correlations in an orchard-grown population of trees segregating for fire blight resistance. Of the 690 transcripts originally identified using the first-generation array, 39 had expression levels that correlated with fire blight resistance in the breeding population.Conclusions: Rootstocks had significant effects on the fire blight susceptibility of 'Gala' scions, and rootstock-regulated gene expression patterns could be correlated with differences in susceptibility. The results suggest a relationship between rootstock-regulated fire blight susceptibility and sorbitol dehydrogenase, phenylpropanoid metabolism, protein processing in the endoplasmic reticulum, and endocytosis, among others. This study illustrates the utility of our rootstock-regulated gene expression data sets for candidate trait-associated gene data mining.

Original languageEnglish (US)
Article number9
JournalBMC Genomics
Volume13
Issue number1
DOIs
StatePublished - Jan 9 2012

Fingerprint

Malus
Gene Expression
Erwinia amylovora
Necrosis
L-Iditol 2-Dehydrogenase
Data Mining
Endocytosis
Oligonucleotide Array Sequence Analysis
Endoplasmic Reticulum
Population
Breeding
Infection
Genes

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Genetics

Cite this

Jensen, Philip J. ; Halbrendt, Noemi ; Fazio, Gennaro ; Makalowska, Izabela ; Altman, Naomi S. ; Praul, Craig ; Maximova, Siela ; Ngugi, Henry K. ; Crassweller, Robert Michael ; Travis, James W. ; McNellis, Timothy W. / Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. In: BMC Genomics. 2012 ; Vol. 13, No. 1.
@article{d322cfcac640439bb20278c2b1f87def,
title = "Rootstock-regulated gene expression patterns associated with fire blight resistance in apple",
abstract = "Background: Desirable apple varieties are clonally propagated by grafting vegetative scions onto rootstocks. Rootstocks influence many phenotypic traits of the scion, including resistance to pathogens such as Erwinia amylovora, which causes fire blight, the most serious bacterial disease of apple. The purpose of the present study was to quantify rootstock-mediated differences in scion fire blight susceptibility and to identify transcripts in the scion whose expression levels correlated with this response.Results: Rootstock influence on scion fire blight resistance was quantified by inoculating three-year old, orchard-grown apple trees, consisting of 'Gala' scions grafted to a range of rootstocks, with E. amylovora. Disease severity was measured by the extent of shoot necrosis over time. 'Gala' scions grafted to G.30 or MM.111 rootstocks showed the lowest rates of necrosis, while 'Gala' on M.27 and B.9 showed the highest rates of necrosis. 'Gala' scions on M.7, S.4 or M.9F56 had intermediate necrosis rates. Using an apple DNA microarray representing 55,230 unique transcripts, gene expression patterns were compared in healthy, un-inoculated, greenhouse-grown 'Gala' scions on the same series of rootstocks. We identified 690 transcripts whose steady-state expression levels correlated with the degree of fire blight susceptibility of the scion/rootstock combinations. Transcripts known to be differentially expressed during E. amylovora infection were disproportionately represented among these transcripts. A second-generation apple microarray representing 26,000 transcripts was developed and was used to test these correlations in an orchard-grown population of trees segregating for fire blight resistance. Of the 690 transcripts originally identified using the first-generation array, 39 had expression levels that correlated with fire blight resistance in the breeding population.Conclusions: Rootstocks had significant effects on the fire blight susceptibility of 'Gala' scions, and rootstock-regulated gene expression patterns could be correlated with differences in susceptibility. The results suggest a relationship between rootstock-regulated fire blight susceptibility and sorbitol dehydrogenase, phenylpropanoid metabolism, protein processing in the endoplasmic reticulum, and endocytosis, among others. This study illustrates the utility of our rootstock-regulated gene expression data sets for candidate trait-associated gene data mining.",
author = "Jensen, {Philip J.} and Noemi Halbrendt and Gennaro Fazio and Izabela Makalowska and Altman, {Naomi S.} and Craig Praul and Siela Maximova and Ngugi, {Henry K.} and Crassweller, {Robert Michael} and Travis, {James W.} and McNellis, {Timothy W.}",
year = "2012",
month = "1",
day = "9",
doi = "10.1186/1471-2164-13-9",
language = "English (US)",
volume = "13",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",
number = "1",

}

Jensen, PJ, Halbrendt, N, Fazio, G, Makalowska, I, Altman, NS, Praul, C, Maximova, S, Ngugi, HK, Crassweller, RM, Travis, JW & McNellis, TW 2012, 'Rootstock-regulated gene expression patterns associated with fire blight resistance in apple', BMC Genomics, vol. 13, no. 1, 9. https://doi.org/10.1186/1471-2164-13-9

Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. / Jensen, Philip J.; Halbrendt, Noemi; Fazio, Gennaro; Makalowska, Izabela; Altman, Naomi S.; Praul, Craig; Maximova, Siela; Ngugi, Henry K.; Crassweller, Robert Michael; Travis, James W.; McNellis, Timothy W.

In: BMC Genomics, Vol. 13, No. 1, 9, 09.01.2012.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Rootstock-regulated gene expression patterns associated with fire blight resistance in apple

AU - Jensen, Philip J.

AU - Halbrendt, Noemi

AU - Fazio, Gennaro

AU - Makalowska, Izabela

AU - Altman, Naomi S.

AU - Praul, Craig

AU - Maximova, Siela

AU - Ngugi, Henry K.

AU - Crassweller, Robert Michael

AU - Travis, James W.

AU - McNellis, Timothy W.

PY - 2012/1/9

Y1 - 2012/1/9

N2 - Background: Desirable apple varieties are clonally propagated by grafting vegetative scions onto rootstocks. Rootstocks influence many phenotypic traits of the scion, including resistance to pathogens such as Erwinia amylovora, which causes fire blight, the most serious bacterial disease of apple. The purpose of the present study was to quantify rootstock-mediated differences in scion fire blight susceptibility and to identify transcripts in the scion whose expression levels correlated with this response.Results: Rootstock influence on scion fire blight resistance was quantified by inoculating three-year old, orchard-grown apple trees, consisting of 'Gala' scions grafted to a range of rootstocks, with E. amylovora. Disease severity was measured by the extent of shoot necrosis over time. 'Gala' scions grafted to G.30 or MM.111 rootstocks showed the lowest rates of necrosis, while 'Gala' on M.27 and B.9 showed the highest rates of necrosis. 'Gala' scions on M.7, S.4 or M.9F56 had intermediate necrosis rates. Using an apple DNA microarray representing 55,230 unique transcripts, gene expression patterns were compared in healthy, un-inoculated, greenhouse-grown 'Gala' scions on the same series of rootstocks. We identified 690 transcripts whose steady-state expression levels correlated with the degree of fire blight susceptibility of the scion/rootstock combinations. Transcripts known to be differentially expressed during E. amylovora infection were disproportionately represented among these transcripts. A second-generation apple microarray representing 26,000 transcripts was developed and was used to test these correlations in an orchard-grown population of trees segregating for fire blight resistance. Of the 690 transcripts originally identified using the first-generation array, 39 had expression levels that correlated with fire blight resistance in the breeding population.Conclusions: Rootstocks had significant effects on the fire blight susceptibility of 'Gala' scions, and rootstock-regulated gene expression patterns could be correlated with differences in susceptibility. The results suggest a relationship between rootstock-regulated fire blight susceptibility and sorbitol dehydrogenase, phenylpropanoid metabolism, protein processing in the endoplasmic reticulum, and endocytosis, among others. This study illustrates the utility of our rootstock-regulated gene expression data sets for candidate trait-associated gene data mining.

AB - Background: Desirable apple varieties are clonally propagated by grafting vegetative scions onto rootstocks. Rootstocks influence many phenotypic traits of the scion, including resistance to pathogens such as Erwinia amylovora, which causes fire blight, the most serious bacterial disease of apple. The purpose of the present study was to quantify rootstock-mediated differences in scion fire blight susceptibility and to identify transcripts in the scion whose expression levels correlated with this response.Results: Rootstock influence on scion fire blight resistance was quantified by inoculating three-year old, orchard-grown apple trees, consisting of 'Gala' scions grafted to a range of rootstocks, with E. amylovora. Disease severity was measured by the extent of shoot necrosis over time. 'Gala' scions grafted to G.30 or MM.111 rootstocks showed the lowest rates of necrosis, while 'Gala' on M.27 and B.9 showed the highest rates of necrosis. 'Gala' scions on M.7, S.4 or M.9F56 had intermediate necrosis rates. Using an apple DNA microarray representing 55,230 unique transcripts, gene expression patterns were compared in healthy, un-inoculated, greenhouse-grown 'Gala' scions on the same series of rootstocks. We identified 690 transcripts whose steady-state expression levels correlated with the degree of fire blight susceptibility of the scion/rootstock combinations. Transcripts known to be differentially expressed during E. amylovora infection were disproportionately represented among these transcripts. A second-generation apple microarray representing 26,000 transcripts was developed and was used to test these correlations in an orchard-grown population of trees segregating for fire blight resistance. Of the 690 transcripts originally identified using the first-generation array, 39 had expression levels that correlated with fire blight resistance in the breeding population.Conclusions: Rootstocks had significant effects on the fire blight susceptibility of 'Gala' scions, and rootstock-regulated gene expression patterns could be correlated with differences in susceptibility. The results suggest a relationship between rootstock-regulated fire blight susceptibility and sorbitol dehydrogenase, phenylpropanoid metabolism, protein processing in the endoplasmic reticulum, and endocytosis, among others. This study illustrates the utility of our rootstock-regulated gene expression data sets for candidate trait-associated gene data mining.

UR - http://www.scopus.com/inward/record.url?scp=84855495228&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84855495228&partnerID=8YFLogxK

U2 - 10.1186/1471-2164-13-9

DO - 10.1186/1471-2164-13-9

M3 - Article

VL - 13

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 9

ER -

Jensen PJ, Halbrendt N, Fazio G, Makalowska I, Altman NS, Praul C et al. Rootstock-regulated gene expression patterns associated with fire blight resistance in apple. BMC Genomics. 2012 Jan 9;13(1). 9. https://doi.org/10.1186/1471-2164-13-9