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Title: Transporters involved in pH and K + homeostasis affect pollen wall formation, male fertility, and embryo development

Abstract

Flowering plant genomes encode multiple cation/H + exchangers (CHXs) whose functions are largely unknown. AtCHX17, AtCHX18, and AtCHX19 are membrane transporters that modulate K+ and pH homeostasis and are localized in the dynamic endomembrane system. Loss of function reduced seed set, but the particular phase(s) of reproduction affected was not determined. Pollen tube growth and ovule targeting of chx17chx18chx19 mutant pollen appeared normal, but reciprocal cross experiments indicate a largely male defect. Although triple mutant pollen tubes reach ovules of a wild-type pistil and a synergid cell degenerated, half of those ovules were unfertilized or showed fertilization of the egg or central cell, but not both female gametes. Fertility could be partially compromised by impaired pollen tube and/or sperm function as CHX19 and CHX18 are expressed in the pollen tube and sperm cell, respectively. When fertilization was successful in self-pollinated mutants, early embryo formation was retarded compared with embryos from wild-type ovules receiving mutant pollen. Thus CHX17 and CHX18 proteins may promote embryo development possibly through the endosperm where these genes are expressed. The reticulate pattern of the pollen wall was disorganized in triple mutants, indicating perturbation of wall formation during male gametophyte development. Lastly, as pH and cation homeostasismore » mediated by AtCHX17 affect membrane trafficking and cargo delivery, these results suggest that male fertility, sperm function, and embryo development are dependent on proper cargo sorting and secretion that remodel cell walls, plasma membranes, and extracellular factors.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [1];  [3];  [4];  [3];  [2]; ORCiD logo [1]
  1. Univ. of Maryland, College Park, MD (United States)
  2. Brown Univ., Providence, RI (United States)
  3. Univ. of Massachusetts, Amherst, MA (United States)
  4. Univ. of Maryland, College Park, MD (United States); Burapha Univ., Chon-Buri (Thailand)
Publication Date:
Research Org.:
Univ. of Maryland, College Park, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
Contributing Org.:
University of Maryland
OSTI Identifier:
1351083
Grant/Contract Number:
FG02-07ER15883
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Volume: 68; Journal Issue: 12; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cation; endomembrane; male fertility; pollen; proton; transport; wall formation

Citation Formats

Padmanaban, Senthilkumar, Czerny, Daniel D., Levin, Kara A., Leydon, Alexander R., Su, Robert T., Maugel, Timothy K., Zou, Yanjiao, Chanroj, Salil, Cheung, Alice Y., Johnson, Mark A., and Sze, Heven. Transporters involved in pH and K+ homeostasis affect pollen wall formation, male fertility, and embryo development. United States: N. p., 2017. Web. doi:10.1093/jxb/erw483.
Padmanaban, Senthilkumar, Czerny, Daniel D., Levin, Kara A., Leydon, Alexander R., Su, Robert T., Maugel, Timothy K., Zou, Yanjiao, Chanroj, Salil, Cheung, Alice Y., Johnson, Mark A., & Sze, Heven. Transporters involved in pH and K+ homeostasis affect pollen wall formation, male fertility, and embryo development. United States. doi:10.1093/jxb/erw483.
Padmanaban, Senthilkumar, Czerny, Daniel D., Levin, Kara A., Leydon, Alexander R., Su, Robert T., Maugel, Timothy K., Zou, Yanjiao, Chanroj, Salil, Cheung, Alice Y., Johnson, Mark A., and Sze, Heven. Thu . "Transporters involved in pH and K+ homeostasis affect pollen wall formation, male fertility, and embryo development". United States. doi:10.1093/jxb/erw483. https://www.osti.gov/servlets/purl/1351083.
@article{osti_1351083,
title = {Transporters involved in pH and K+ homeostasis affect pollen wall formation, male fertility, and embryo development},
author = {Padmanaban, Senthilkumar and Czerny, Daniel D. and Levin, Kara A. and Leydon, Alexander R. and Su, Robert T. and Maugel, Timothy K. and Zou, Yanjiao and Chanroj, Salil and Cheung, Alice Y. and Johnson, Mark A. and Sze, Heven},
abstractNote = {Flowering plant genomes encode multiple cation/H+ exchangers (CHXs) whose functions are largely unknown. AtCHX17, AtCHX18, and AtCHX19 are membrane transporters that modulate K+ and pH homeostasis and are localized in the dynamic endomembrane system. Loss of function reduced seed set, but the particular phase(s) of reproduction affected was not determined. Pollen tube growth and ovule targeting of chx17chx18chx19 mutant pollen appeared normal, but reciprocal cross experiments indicate a largely male defect. Although triple mutant pollen tubes reach ovules of a wild-type pistil and a synergid cell degenerated, half of those ovules were unfertilized or showed fertilization of the egg or central cell, but not both female gametes. Fertility could be partially compromised by impaired pollen tube and/or sperm function as CHX19 and CHX18 are expressed in the pollen tube and sperm cell, respectively. When fertilization was successful in self-pollinated mutants, early embryo formation was retarded compared with embryos from wild-type ovules receiving mutant pollen. Thus CHX17 and CHX18 proteins may promote embryo development possibly through the endosperm where these genes are expressed. The reticulate pattern of the pollen wall was disorganized in triple mutants, indicating perturbation of wall formation during male gametophyte development. Lastly, as pH and cation homeostasis mediated by AtCHX17 affect membrane trafficking and cargo delivery, these results suggest that male fertility, sperm function, and embryo development are dependent on proper cargo sorting and secretion that remodel cell walls, plasma membranes, and extracellular factors.},
doi = {10.1093/jxb/erw483},
journal = {Journal of Experimental Botany},
number = 12,
volume = 68,
place = {United States},
year = {Thu Feb 23 00:00:00 EST 2017},
month = {Thu Feb 23 00:00:00 EST 2017}
}

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