In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling

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Abstract

Main conclusion: A conserved UPR machinery is required forBrachypodiumER stress resistance and grain filling.Human and livestock diets depend on the accumulation of cereal storage proteins and carbohydrates, including mixed-linkage glucan (MLG), in the endosperm during seed development. Storage proteins and proteins responsible for the production of carbohydrates are synthesized in the endoplasmic reticulum (ER). Unfavorable conditions during growth that hamper the ER biosynthetic capacity, such as heat, can cause a potentially lethal condition known as ER stress, which activates the unfolded protein response (UPR), a signaling response designed to mitigate ER stress. The UPR relies primarily on a conserved ER-associated kinase and ribonuclease, IRE1, which splices the mRNA of a transcription factor (TF), such as bZIP60 in plants, to produce an active TF that controls the expression of ER resident chaperones. Here, we investigated activation of the UPR in Brachypodium, as a model to study the UPR in seeds of a monocotyledon species, as well as the consequences of heat stress on MLG deposition in seeds. We identified a Brachypodium bZIP60 orthologue and determined a positive correlation between bZIP60 splicing and ER stress induced by chemicals and heat. Each stress condition led to transcriptional modulation of several BiP genes, supporting the existence of condition-specific BiP regulation. Finally, we found that the UPR is elevated at the early stage of seed development and that MLG production is negatively affected by heat stress via modulation of MLG synthase accumulation. We propose that successful accomplishment of seed filling is strongly correlated with the ability of the plant to sustain ER stress via the UPR.

LanguageEnglish (US)
Pages1-15
Number of pages15
JournalPlanta
DOIs
StateAccepted/In press - Mar 31 2017

Profile

Brachypodium
Unfolded Protein Response
unfolded protein response
filling period
endoplasmic reticulum
Seeds
Endoplasmic Reticulum Stress
Endoplasmic Reticulum
glucans
Glucans
linkage (genetics)
Hot Temperature
cells
storage proteins
seed development
Transcription Factors
heat stress
Carbohydrates
transcription factors
Endosperm

Keywords

  • bZIP60
  • Endosperm
  • ER stress
  • Heat stress
  • Mixed-linkage glucan

ASJC Scopus subject areas

  • Genetics
  • Plant Science

Cite this

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title = "In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling",
abstract = "Main conclusion: A conserved UPR machinery is required forBrachypodiumER stress resistance and grain filling.Human and livestock diets depend on the accumulation of cereal storage proteins and carbohydrates, including mixed-linkage glucan (MLG), in the endosperm during seed development. Storage proteins and proteins responsible for the production of carbohydrates are synthesized in the endoplasmic reticulum (ER). Unfavorable conditions during growth that hamper the ER biosynthetic capacity, such as heat, can cause a potentially lethal condition known as ER stress, which activates the unfolded protein response (UPR), a signaling response designed to mitigate ER stress. The UPR relies primarily on a conserved ER-associated kinase and ribonuclease, IRE1, which splices the mRNA of a transcription factor (TF), such as bZIP60 in plants, to produce an active TF that controls the expression of ER resident chaperones. Here, we investigated activation of the UPR in Brachypodium, as a model to study the UPR in seeds of a monocotyledon species, as well as the consequences of heat stress on MLG deposition in seeds. We identified a Brachypodium bZIP60 orthologue and determined a positive correlation between bZIP60 splicing and ER stress induced by chemicals and heat. Each stress condition led to transcriptional modulation of several BiP genes, supporting the existence of condition-specific BiP regulation. Finally, we found that the UPR is elevated at the early stage of seed development and that MLG production is negatively affected by heat stress via modulation of MLG synthase accumulation. We propose that successful accomplishment of seed filling is strongly correlated with the ability of the plant to sustain ER stress via the UPR.",
keywords = "bZIP60, Endosperm, ER stress, Heat stress, Mixed-linkage glucan",
author = "Kim, {Sang Jin} and Starla Zemelis-Durfee and Curtis Wilkerson and Federica Brandizzi",
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AU - Kim,Sang Jin

AU - Zemelis-Durfee,Starla

AU - Wilkerson,Curtis

AU - Brandizzi,Federica

PY - 2017/3/31

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N2 - Main conclusion: A conserved UPR machinery is required forBrachypodiumER stress resistance and grain filling.Human and livestock diets depend on the accumulation of cereal storage proteins and carbohydrates, including mixed-linkage glucan (MLG), in the endosperm during seed development. Storage proteins and proteins responsible for the production of carbohydrates are synthesized in the endoplasmic reticulum (ER). Unfavorable conditions during growth that hamper the ER biosynthetic capacity, such as heat, can cause a potentially lethal condition known as ER stress, which activates the unfolded protein response (UPR), a signaling response designed to mitigate ER stress. The UPR relies primarily on a conserved ER-associated kinase and ribonuclease, IRE1, which splices the mRNA of a transcription factor (TF), such as bZIP60 in plants, to produce an active TF that controls the expression of ER resident chaperones. Here, we investigated activation of the UPR in Brachypodium, as a model to study the UPR in seeds of a monocotyledon species, as well as the consequences of heat stress on MLG deposition in seeds. We identified a Brachypodium bZIP60 orthologue and determined a positive correlation between bZIP60 splicing and ER stress induced by chemicals and heat. Each stress condition led to transcriptional modulation of several BiP genes, supporting the existence of condition-specific BiP regulation. Finally, we found that the UPR is elevated at the early stage of seed development and that MLG production is negatively affected by heat stress via modulation of MLG synthase accumulation. We propose that successful accomplishment of seed filling is strongly correlated with the ability of the plant to sustain ER stress via the UPR.

AB - Main conclusion: A conserved UPR machinery is required forBrachypodiumER stress resistance and grain filling.Human and livestock diets depend on the accumulation of cereal storage proteins and carbohydrates, including mixed-linkage glucan (MLG), in the endosperm during seed development. Storage proteins and proteins responsible for the production of carbohydrates are synthesized in the endoplasmic reticulum (ER). Unfavorable conditions during growth that hamper the ER biosynthetic capacity, such as heat, can cause a potentially lethal condition known as ER stress, which activates the unfolded protein response (UPR), a signaling response designed to mitigate ER stress. The UPR relies primarily on a conserved ER-associated kinase and ribonuclease, IRE1, which splices the mRNA of a transcription factor (TF), such as bZIP60 in plants, to produce an active TF that controls the expression of ER resident chaperones. Here, we investigated activation of the UPR in Brachypodium, as a model to study the UPR in seeds of a monocotyledon species, as well as the consequences of heat stress on MLG deposition in seeds. We identified a Brachypodium bZIP60 orthologue and determined a positive correlation between bZIP60 splicing and ER stress induced by chemicals and heat. Each stress condition led to transcriptional modulation of several BiP genes, supporting the existence of condition-specific BiP regulation. Finally, we found that the UPR is elevated at the early stage of seed development and that MLG production is negatively affected by heat stress via modulation of MLG synthase accumulation. We propose that successful accomplishment of seed filling is strongly correlated with the ability of the plant to sustain ER stress via the UPR.

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