Glycolysis regulates pollen tube polarity via Rho GTPase signaling.
As a universal energy generation pathway utilizing carbon metabolism, glycolysis plays an important housekeeping role in all organisms. Pollen tubes expand rapidly via a mechanism of polarized growth, known as tip growth, to deliver sperm for fertilization. Here, we report a novel and surprising rol...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2018-04-01
|
| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC5942846?pdf=render |
| _version_ | 1811336874467262464 |
|---|---|
| author | Wei Chen Pingping Gong Jingzhe Guo Hui Li Ruizi Li Weiman Xing Zhenbiao Yang Yuefeng Guan |
| author_facet | Wei Chen Pingping Gong Jingzhe Guo Hui Li Ruizi Li Weiman Xing Zhenbiao Yang Yuefeng Guan |
| author_sort | Wei Chen |
| collection | DOAJ |
| description | As a universal energy generation pathway utilizing carbon metabolism, glycolysis plays an important housekeeping role in all organisms. Pollen tubes expand rapidly via a mechanism of polarized growth, known as tip growth, to deliver sperm for fertilization. Here, we report a novel and surprising role of glycolysis in the regulation of growth polarity in Arabidopsis pollen tubes via impingement of Rho GTPase-dependent signaling. We identified a cytosolic phosphoglycerate kinase (pgkc-1) mutant with accelerated pollen germination and compromised pollen tube growth polarity. pgkc-1 mutation greatly diminished apical exocytic vesicular distribution of REN1 RopGAP (Rop GTPase activating protein), leading to ROP1 hyper-activation at the apical plasma membrane. Consequently, pgkc-1 pollen tubes contained higher amounts of exocytic vesicles and actin microfilaments in the apical region, and showed reduced sensitivity to Brefeldin A and Latrunculin B, respectively. While inhibition of mitochondrial respiration could not explain the pgkc-1 phenotype, the glycolytic activity is indeed required for PGKc function in pollen tubes. Moreover, the pgkc-1 pollen tube phenotype was mimicked by the inhibition of another glycolytic enzyme. These findings highlight an unconventional regulatory function for a housekeeping metabolic pathway in the spatial control of a fundamental cellular process. |
| first_indexed | 2024-04-13T17:45:53Z |
| format | Article |
| id | doaj.art-3b3f1a8a23df48769fa2346c901a2ecb |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-13T17:45:53Z |
| publishDate | 2018-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-3b3f1a8a23df48769fa2346c901a2ecb2022-12-22T02:36:57ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042018-04-01144e100737310.1371/journal.pgen.1007373Glycolysis regulates pollen tube polarity via Rho GTPase signaling.Wei ChenPingping GongJingzhe GuoHui LiRuizi LiWeiman XingZhenbiao YangYuefeng GuanAs a universal energy generation pathway utilizing carbon metabolism, glycolysis plays an important housekeeping role in all organisms. Pollen tubes expand rapidly via a mechanism of polarized growth, known as tip growth, to deliver sperm for fertilization. Here, we report a novel and surprising role of glycolysis in the regulation of growth polarity in Arabidopsis pollen tubes via impingement of Rho GTPase-dependent signaling. We identified a cytosolic phosphoglycerate kinase (pgkc-1) mutant with accelerated pollen germination and compromised pollen tube growth polarity. pgkc-1 mutation greatly diminished apical exocytic vesicular distribution of REN1 RopGAP (Rop GTPase activating protein), leading to ROP1 hyper-activation at the apical plasma membrane. Consequently, pgkc-1 pollen tubes contained higher amounts of exocytic vesicles and actin microfilaments in the apical region, and showed reduced sensitivity to Brefeldin A and Latrunculin B, respectively. While inhibition of mitochondrial respiration could not explain the pgkc-1 phenotype, the glycolytic activity is indeed required for PGKc function in pollen tubes. Moreover, the pgkc-1 pollen tube phenotype was mimicked by the inhibition of another glycolytic enzyme. These findings highlight an unconventional regulatory function for a housekeeping metabolic pathway in the spatial control of a fundamental cellular process.http://europepmc.org/articles/PMC5942846?pdf=render |
| spellingShingle | Wei Chen Pingping Gong Jingzhe Guo Hui Li Ruizi Li Weiman Xing Zhenbiao Yang Yuefeng Guan Glycolysis regulates pollen tube polarity via Rho GTPase signaling. PLoS Genetics |
| title | Glycolysis regulates pollen tube polarity via Rho GTPase signaling. |
| title_full | Glycolysis regulates pollen tube polarity via Rho GTPase signaling. |
| title_fullStr | Glycolysis regulates pollen tube polarity via Rho GTPase signaling. |
| title_full_unstemmed | Glycolysis regulates pollen tube polarity via Rho GTPase signaling. |
| title_short | Glycolysis regulates pollen tube polarity via Rho GTPase signaling. |
| title_sort | glycolysis regulates pollen tube polarity via rho gtpase signaling |
| url | http://europepmc.org/articles/PMC5942846?pdf=render |
| work_keys_str_mv | AT weichen glycolysisregulatespollentubepolarityviarhogtpasesignaling AT pingpinggong glycolysisregulatespollentubepolarityviarhogtpasesignaling AT jingzheguo glycolysisregulatespollentubepolarityviarhogtpasesignaling AT huili glycolysisregulatespollentubepolarityviarhogtpasesignaling AT ruizili glycolysisregulatespollentubepolarityviarhogtpasesignaling AT weimanxing glycolysisregulatespollentubepolarityviarhogtpasesignaling AT zhenbiaoyang glycolysisregulatespollentubepolarityviarhogtpasesignaling AT yuefengguan glycolysisregulatespollentubepolarityviarhogtpasesignaling |