Paper · 2023 · The Plant Cell

BOTRYOID POLLEN 1 regulates ROS-triggered PCD and pollen wall development by controlling UDP-sugar homeostasis in rice

Huiqiong Chen; Shuqing Zhang; Ruiqi Li; et al.

10
claims
19
verbatim quotes
49
citations
3
research areas
✓
Open access

Abstract

Uridine diphosphate (UDP)-sugars are important metabolites involved in the biosynthesis of polysaccharides and may be important signaling molecules. UDP-glucose 4-epimerase (UGE) catalyzes the interconversion between UDP-Glc and UDP-Gal, whose biological function in rice (Oryza sativa) fertility is poorly understood. Here, we identify and characterize the botryoid pollen 1 (bp1) mutant and show that BP1 encodes a UGE that regulates UDP-sugar homeostasis, thereby controlling the development of rice anthers. The loss of BP1 function led to massive accumulation of UDP-Glc and imbalance of other UDP-sugars. We determined that the higher levels of UDP-Glc and its derivatives in bp1 may induce the expression of NADPH oxidase genes, resulting in a premature accumulation of reactive oxygen species (ROS), thereby advancing programmed cell death (PCD) of anther walls but delaying the end of tapetal degradation. The accumulation of UDP-Glc as metabolites resulted in an abnormal degradation of callose, producing an adhesive microspore. Furthermore, the UDP-sugar metabolism pathway is not only involved in the formation of intine but also in the formation of the initial framework for extine. Our results reveal how UDP-sugars regulate anther development and provide new clues for cellular ROS accumulation and PCD triggered by UDP-Glc as a signaling molecule.

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Claims 10

Mechanismobservedoriginal resultmeasured

Claim · model-written summary

BP1 encodes a UGE that regulates UDP-sugar homeostasis and rice anther development.

Gene
BP1e0
Compound
UDP-sugare0
Outcome
development of rice antherse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“BP1 encodes a UGE that regulates UDP-sugar homeostasis, thereby controlling the development of rice anthers”

✓ located verbatim in the source · abstract, characters 403–510 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Loss of BP1 caused massive UDP-Glc accumulation.

Treatment
loss of BP1 functione0
Gene
BP1e0
Outcome
accumulation of UDP-Glce0
Direction
massive accumulatione0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“The loss of BP1 function led to massive accumulation of UDP-Glc”

✓ located verbatim in the source · abstract, characters 512–575 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Loss of BP1 disrupted other UDP-sugars.

Treatment
loss of BP1 functione0
Gene
BP1e0
Outcome
imbalance of other UDP-sugarse0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“The loss of BP1 function led to massive accumulation of UDP-Glc and imbalance of other UDP-sugars”

✓ located verbatim in the source · abstract, characters 512–609 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Mechanismhypothesisoriginal resultnegativemeasured

Claim · model-written summary

Elevated UDP-Glc and its derivatives in bp1 may induce NADPH oxidase gene expression.

Material
bp1e0
Gene
NADPH oxidase genese0
Compound
UDP-Glce0
Outcome
expression of NADPH oxidase genese0
Direction
inducee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“the higher levels of UDP-Glc and its derivatives in bp1 may induce the expression of NADPH oxidase genes”

✓ located verbatim in the source · abstract, characters 630–734 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Mechanismhypothesisoriginal resultnegativemeasured

Claim · model-written summary

Higher UDP-Glc in bp1 may cause premature ROS accumulation.

Material
bp1e0
Compound
UDP-Glce0
Outcome
premature accumulation of reactive oxygen species (ROS)e0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“the higher levels of UDP-Glc and its derivatives in bp1 may induce the expression of NADPH oxidase genes, resulting in a premature accumulation of reactive oxygen species (ROS)”

✓ located verbatim in the source · abstract, characters 630–806 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

The bp1 signaling change advanced anther-wall PCD.

Organ / stage
anther wallse0
Outcome
programmed cell death (PCD) of anther wallse0
Qualifier
thereby advancinge0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“thereby advancing programmed cell death (PCD) of anther walls”

✓ located verbatim in the source · abstract, characters 808–869 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

The bp1 signaling change delayed the end of tapetal degradation.

Organ / stage
tapetale0
Outcome
end of tapetal degradatione0
Qualifier
delayinge0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“delaying the end of tapetal degradation”

✓ located verbatim in the source · abstract, characters 874–913 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Mechanismobservedoriginal resultnegativemeasured

Claim · model-written summary

UDP-Glc accumulation caused abnormal callose degradation and adhesive microspores.

Compound
UDP-Glce0
Outcome
abnormal degradation of callose, producing an adhesive microsporee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“The accumulation of UDP-Glc as metabolites resulted in an abnormal degradation of callose, producing an adhesive microspore.”

✓ located verbatim in the source · abstract, characters 915–1039 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The UDP-sugar metabolism pathway participates in intine formation.

Compound
UDP-sugare0
Outcome
formation of intinee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“the UDP-sugar metabolism pathway is not only involved in the formation of intine but also in the formation of the initial framework for extine”

✓ located verbatim in the source · abstract, characters 1053–1195 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The UDP-sugar metabolism pathway participates in the initial extine framework.

Compound
UDP-sugare0
Outcome
formation of the initial framework for extinee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“the UDP-sugar metabolism pathway is not only involved in the formation of intine but also in the formation of the initial framework for extine”

✓ located verbatim in the source · abstract, characters 1053–1195 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 114–118 · show in text ↑