A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1

Daniela S. Floss, S. Karen Gomez, Hee Jin Park, Allyson M. MacLean, Lena M. Müller, Kishor K. Bhattarai, Veronique Lévesque-Tremblay, Ignacio E. Maldonado-Mendoza, Maria J. Harrison

Research output: Contribution to journalArticle

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Abstract

© 2017 Elsevier Ltd During the endosymbiosis formed between plants and arbuscular mycorrhizal (AM) fungi, the root cortical cells are colonized by branched hyphae called arbuscules, which function in nutrient exchange with the plant [1]. Despite their positive function, arbuscules are ephemeral structures, and their development is followed by a degeneration phase, in which the arbuscule and surrounding periarbuscular membrane and matrix gradually disappear from the root cell [2, 3]. Currently, the root cell's role in this process and the underlying regulatory mechanisms are unknown. Here, by using a Medicago truncatula pt4 mutant in which arbuscules degenerate prematurely [4], we identified arbuscule degeneration-associated genes, of which 38% are predicted to encode secreted hydrolases, suggesting a role in disassembly of the arbuscule and interface. Through RNAi and analysis of an insertion mutant, we identified a symbiosis-specific MYB-like transcription factor (MYB1) that suppresses arbuscule degeneration in mtpt4. In myb1, expression of several degeneration-associated genes is reduced. Conversely, in roots constitutively overexpressing MYB1, expression of degeneration-associated genes is increased and subsequent development of symbiosis is impaired. MYB1-regulated gene expression is enhanced by DELLA proteins and is dependent on NSP1 [5], but not NSP2 [6]. Furthermore, MYB1 interacts with DELLA and NSP1. Our data identify a transcriptional program for arbuscule degeneration and reveal that its regulators include MYB1 in association with two transcriptional regulators, NSP1 and DELLA, both of which function in preceding phases of the symbiosis. We propose that the combinatorial use of transcription factors enables the sequential expression of transcriptional programs for arbuscule development and degeneration.
Original languageAmerican English
Pages (from-to)1206-1212
Number of pages7
JournalCurrent Biology
DOIs
StatePublished - 24 Apr 2017
Externally publishedYes

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Symbiosis
symbiosis
Genes
transcription factors
Transcription Factors
Medicago truncatula
Hydrolases
Fungi
Gene expression
mutants
Nutrients
genes
Hyphae
program planning
cells
RNA Interference
hydrolases
hyphae
mycorrhizal fungi
Membranes

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Floss, D. S., Gomez, S. K., Park, H. J., MacLean, A. M., Müller, L. M., Bhattarai, K. K., ... Harrison, M. J. (2017). A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1. Current Biology, 1206-1212. https://doi.org/10.1016/j.cub.2017.03.003
Floss, Daniela S. ; Gomez, S. Karen ; Park, Hee Jin ; MacLean, Allyson M. ; Müller, Lena M. ; Bhattarai, Kishor K. ; Lévesque-Tremblay, Veronique ; Maldonado-Mendoza, Ignacio E. ; Harrison, Maria J. / A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1. In: Current Biology. 2017 ; pp. 1206-1212.
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abstract = "{\circledC} 2017 Elsevier Ltd During the endosymbiosis formed between plants and arbuscular mycorrhizal (AM) fungi, the root cortical cells are colonized by branched hyphae called arbuscules, which function in nutrient exchange with the plant [1]. Despite their positive function, arbuscules are ephemeral structures, and their development is followed by a degeneration phase, in which the arbuscule and surrounding periarbuscular membrane and matrix gradually disappear from the root cell [2, 3]. Currently, the root cell's role in this process and the underlying regulatory mechanisms are unknown. Here, by using a Medicago truncatula pt4 mutant in which arbuscules degenerate prematurely [4], we identified arbuscule degeneration-associated genes, of which 38{\%} are predicted to encode secreted hydrolases, suggesting a role in disassembly of the arbuscule and interface. Through RNAi and analysis of an insertion mutant, we identified a symbiosis-specific MYB-like transcription factor (MYB1) that suppresses arbuscule degeneration in mtpt4. In myb1, expression of several degeneration-associated genes is reduced. Conversely, in roots constitutively overexpressing MYB1, expression of degeneration-associated genes is increased and subsequent development of symbiosis is impaired. MYB1-regulated gene expression is enhanced by DELLA proteins and is dependent on NSP1 [5], but not NSP2 [6]. Furthermore, MYB1 interacts with DELLA and NSP1. Our data identify a transcriptional program for arbuscule degeneration and reveal that its regulators include MYB1 in association with two transcriptional regulators, NSP1 and DELLA, both of which function in preceding phases of the symbiosis. We propose that the combinatorial use of transcription factors enables the sequential expression of transcriptional programs for arbuscule development and degeneration.",
author = "Floss, {Daniela S.} and Gomez, {S. Karen} and Park, {Hee Jin} and MacLean, {Allyson M.} and M{\"u}ller, {Lena M.} and Bhattarai, {Kishor K.} and Veronique L{\'e}vesque-Tremblay and Maldonado-Mendoza, {Ignacio E.} and Harrison, {Maria J.}",
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Floss, DS, Gomez, SK, Park, HJ, MacLean, AM, Müller, LM, Bhattarai, KK, Lévesque-Tremblay, V, Maldonado-Mendoza, IE & Harrison, MJ 2017, 'A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1', Current Biology, pp. 1206-1212. https://doi.org/10.1016/j.cub.2017.03.003

A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1. / Floss, Daniela S.; Gomez, S. Karen; Park, Hee Jin; MacLean, Allyson M.; Müller, Lena M.; Bhattarai, Kishor K.; Lévesque-Tremblay, Veronique; Maldonado-Mendoza, Ignacio E.; Harrison, Maria J.

In: Current Biology, 24.04.2017, p. 1206-1212.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1

AU - Floss, Daniela S.

AU - Gomez, S. Karen

AU - Park, Hee Jin

AU - MacLean, Allyson M.

AU - Müller, Lena M.

AU - Bhattarai, Kishor K.

AU - Lévesque-Tremblay, Veronique

AU - Maldonado-Mendoza, Ignacio E.

AU - Harrison, Maria J.

PY - 2017/4/24

Y1 - 2017/4/24

N2 - © 2017 Elsevier Ltd During the endosymbiosis formed between plants and arbuscular mycorrhizal (AM) fungi, the root cortical cells are colonized by branched hyphae called arbuscules, which function in nutrient exchange with the plant [1]. Despite their positive function, arbuscules are ephemeral structures, and their development is followed by a degeneration phase, in which the arbuscule and surrounding periarbuscular membrane and matrix gradually disappear from the root cell [2, 3]. Currently, the root cell's role in this process and the underlying regulatory mechanisms are unknown. Here, by using a Medicago truncatula pt4 mutant in which arbuscules degenerate prematurely [4], we identified arbuscule degeneration-associated genes, of which 38% are predicted to encode secreted hydrolases, suggesting a role in disassembly of the arbuscule and interface. Through RNAi and analysis of an insertion mutant, we identified a symbiosis-specific MYB-like transcription factor (MYB1) that suppresses arbuscule degeneration in mtpt4. In myb1, expression of several degeneration-associated genes is reduced. Conversely, in roots constitutively overexpressing MYB1, expression of degeneration-associated genes is increased and subsequent development of symbiosis is impaired. MYB1-regulated gene expression is enhanced by DELLA proteins and is dependent on NSP1 [5], but not NSP2 [6]. Furthermore, MYB1 interacts with DELLA and NSP1. Our data identify a transcriptional program for arbuscule degeneration and reveal that its regulators include MYB1 in association with two transcriptional regulators, NSP1 and DELLA, both of which function in preceding phases of the symbiosis. We propose that the combinatorial use of transcription factors enables the sequential expression of transcriptional programs for arbuscule development and degeneration.

AB - © 2017 Elsevier Ltd During the endosymbiosis formed between plants and arbuscular mycorrhizal (AM) fungi, the root cortical cells are colonized by branched hyphae called arbuscules, which function in nutrient exchange with the plant [1]. Despite their positive function, arbuscules are ephemeral structures, and their development is followed by a degeneration phase, in which the arbuscule and surrounding periarbuscular membrane and matrix gradually disappear from the root cell [2, 3]. Currently, the root cell's role in this process and the underlying regulatory mechanisms are unknown. Here, by using a Medicago truncatula pt4 mutant in which arbuscules degenerate prematurely [4], we identified arbuscule degeneration-associated genes, of which 38% are predicted to encode secreted hydrolases, suggesting a role in disassembly of the arbuscule and interface. Through RNAi and analysis of an insertion mutant, we identified a symbiosis-specific MYB-like transcription factor (MYB1) that suppresses arbuscule degeneration in mtpt4. In myb1, expression of several degeneration-associated genes is reduced. Conversely, in roots constitutively overexpressing MYB1, expression of degeneration-associated genes is increased and subsequent development of symbiosis is impaired. MYB1-regulated gene expression is enhanced by DELLA proteins and is dependent on NSP1 [5], but not NSP2 [6]. Furthermore, MYB1 interacts with DELLA and NSP1. Our data identify a transcriptional program for arbuscule degeneration and reveal that its regulators include MYB1 in association with two transcriptional regulators, NSP1 and DELLA, both of which function in preceding phases of the symbiosis. We propose that the combinatorial use of transcription factors enables the sequential expression of transcriptional programs for arbuscule development and degeneration.

U2 - 10.1016/j.cub.2017.03.003

DO - 10.1016/j.cub.2017.03.003

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Floss DS, Gomez SK, Park HJ, MacLean AM, Müller LM, Bhattarai KK et al. A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1. Current Biology. 2017 Apr 24;1206-1212. https://doi.org/10.1016/j.cub.2017.03.003