Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in Arabidopsis

Abstract Background Starch is synthesized during daylight for temporary storage in leaves and then degraded during the subsequent night to support plant growth and development. Impairment of starch degradation leads to stunted growth, even senescence and death. The nuclear pore complex is involved i...

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Main Authors: Long Xiao, Shanshan Jiang, Penghui Huang, Fulu Chen, Xu Wang, Zhiyuan Cheng, Yuchen Miao, Liangyu Liu, Iain Searle, Chunyan Liu, Xiao-Xia Wu, Yong-Fu Fu, Qingshan Chen, Xiao-Mei Zhang
Format: Article
Language:English
Published: BMC 2020-06-01
Series:BMC Plant Biology
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Online Access:http://link.springer.com/article/10.1186/s12870-020-02494-1
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author Long Xiao
Shanshan Jiang
Penghui Huang
Fulu Chen
Xu Wang
Zhiyuan Cheng
Yuchen Miao
Liangyu Liu
Iain Searle
Chunyan Liu
Xiao-Xia Wu
Yong-Fu Fu
Qingshan Chen
Xiao-Mei Zhang
author_facet Long Xiao
Shanshan Jiang
Penghui Huang
Fulu Chen
Xu Wang
Zhiyuan Cheng
Yuchen Miao
Liangyu Liu
Iain Searle
Chunyan Liu
Xiao-Xia Wu
Yong-Fu Fu
Qingshan Chen
Xiao-Mei Zhang
author_sort Long Xiao
collection DOAJ
description Abstract Background Starch is synthesized during daylight for temporary storage in leaves and then degraded during the subsequent night to support plant growth and development. Impairment of starch degradation leads to stunted growth, even senescence and death. The nuclear pore complex is involved in many cellular processes, but its relationship with starch degradation has been unclear until now. We previously identified that two Nucleoporin98 genes (Nup98a and Nup98b) redundantly regulate flowering via the CONSTANS (CO)-independent pathway in Arabidopsis thaliana. The double mutant also shows severe senescence phenotypes. Results We find that Nucleoporin 98 participates in the regulation of sugar metabolism in leaves and is also involved in senescence regulation in Arabidopsis. We show that Nup98a and Nup98b function redundantly at different stages of starch degradation. The nup98a-1 nup98b-1 double mutant accumulates more starch, showing a severe early senescence phenotype compared to wild type plants. The expression of marker genes related to starch degradation is impaired in the nup98a-1 nup98b-1 double mutant, and marker genes of carbon starvation and senescence express their products earlier and in higher abundance than in wild type plants, suggesting that abnormalities in energy metabolism are the main cause of senescence in the double mutant. Addition of sucrose to the growth medium rescues early senescence phenotypes of the nup98a-1 nup98b-1 mutant. Conclusions Our results provide evidence for a novel role of the nuclear pore complex in energy metabolism related to growth and development, in which Nup98 functions in starch degradation to control growth regulation in Arabidopsis.
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spelling doaj.art-a0147d023bda468ea54afa9fd1e7d13a2022-12-22T01:22:41ZengBMCBMC Plant Biology1471-22292020-06-0120111510.1186/s12870-020-02494-1Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in ArabidopsisLong Xiao0Shanshan Jiang1Penghui Huang2Fulu Chen3Xu Wang4Zhiyuan Cheng5Yuchen Miao6Liangyu Liu7Iain Searle8Chunyan Liu9Xiao-Xia Wu10Yong-Fu Fu11Qingshan Chen12Xiao-Mei Zhang13Key Laboratory of Soybean Biology, Ministry of Education/College of Agriculture, Northeast Agricultural UniversityMOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural SciencesMOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural SciencesMOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural SciencesMOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural SciencesMOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Plant Stress Biology, State Key Laboratory of Cotton Biology, School of Life Sciences, Henan UniversityCollege of Life Sciences, Capital Normal UniversitySchool of Biological Sciences, School of Agriculture, Food and Wine, The University of AdelaideKey Laboratory of Soybean Biology, Ministry of Education/College of Agriculture, Northeast Agricultural UniversityKey Laboratory of Soybean Biology, Ministry of Education/College of Agriculture, Northeast Agricultural UniversityMOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Soybean Biology, Ministry of Education/College of Agriculture, Northeast Agricultural UniversityMOA Key Lab of Soybean Biology (Beijing), National Key Facility of Crop Gene Resource and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural SciencesAbstract Background Starch is synthesized during daylight for temporary storage in leaves and then degraded during the subsequent night to support plant growth and development. Impairment of starch degradation leads to stunted growth, even senescence and death. The nuclear pore complex is involved in many cellular processes, but its relationship with starch degradation has been unclear until now. We previously identified that two Nucleoporin98 genes (Nup98a and Nup98b) redundantly regulate flowering via the CONSTANS (CO)-independent pathway in Arabidopsis thaliana. The double mutant also shows severe senescence phenotypes. Results We find that Nucleoporin 98 participates in the regulation of sugar metabolism in leaves and is also involved in senescence regulation in Arabidopsis. We show that Nup98a and Nup98b function redundantly at different stages of starch degradation. The nup98a-1 nup98b-1 double mutant accumulates more starch, showing a severe early senescence phenotype compared to wild type plants. The expression of marker genes related to starch degradation is impaired in the nup98a-1 nup98b-1 double mutant, and marker genes of carbon starvation and senescence express their products earlier and in higher abundance than in wild type plants, suggesting that abnormalities in energy metabolism are the main cause of senescence in the double mutant. Addition of sucrose to the growth medium rescues early senescence phenotypes of the nup98a-1 nup98b-1 mutant. Conclusions Our results provide evidence for a novel role of the nuclear pore complex in energy metabolism related to growth and development, in which Nup98 functions in starch degradation to control growth regulation in Arabidopsis.http://link.springer.com/article/10.1186/s12870-020-02494-1Nup98StarchSugarSenescenceNuclear pore complexNucleoporin
spellingShingle Long Xiao
Shanshan Jiang
Penghui Huang
Fulu Chen
Xu Wang
Zhiyuan Cheng
Yuchen Miao
Liangyu Liu
Iain Searle
Chunyan Liu
Xiao-Xia Wu
Yong-Fu Fu
Qingshan Chen
Xiao-Mei Zhang
Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in Arabidopsis
BMC Plant Biology
Nup98
Starch
Sugar
Senescence
Nuclear pore complex
Nucleoporin
title Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in Arabidopsis
title_full Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in Arabidopsis
title_fullStr Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in Arabidopsis
title_full_unstemmed Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in Arabidopsis
title_short Two Nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in Arabidopsis
title_sort two nucleoporin98 homologous genes jointly participate in the regulation of starch degradation to repress senescence in arabidopsis
topic Nup98
Starch
Sugar
Senescence
Nuclear pore complex
Nucleoporin
url http://link.springer.com/article/10.1186/s12870-020-02494-1
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