4.8 Article

Glucuronidation of type II arabinogalactan polysaccharides function in sexual reproduction of Arabidopsis

Journal

PLANT JOURNAL
Volume 109, Issue 1, Pages 164-181

Publisher

WILEY
DOI: 10.1111/tpj.15562

Keywords

arabinogalactan protein; glucuronosyltransferases; glucuronic acid; polytubey; embryo; mutant; seed set

Categories

Funding

  1. Ohio University (OU) Student Enhancement Award
  2. OU College of Arts and Science Graduate Student Research Fund
  3. OU Nanoscale & Quantum Phenomena Institute (NQPI) fellowship
  4. NIFA-USDA-AFRI Exploratory Research Program [2019-67030-29670]
  5. Research Facilities Improvement Program from the National Center for Research Resources, National Institutes of Health [C06 RR-014575-01]

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Through biochemical and immunolabeling techniques, it was demonstrated that the enzymes GLCAT14A, GLCAT14B, and GLCAT14C play essential roles in pollen development, polytubey block, and normal embryo development in Arabidopsis. Their loss of function resulted in structural abnormalities in pollen grains, disrupted anther development, and compromised mechanisms in sexual reproduction.
Arabinogalactan proteins (AGPs) are complex, hyperglycosylated plant cell wall proteins with little known about the biological roles of their glycan moieties in sexual reproduction. Here, we report that GLCAT14A, GLCAT14B, and GLCAT14C, three enzymes responsible for the addition of glucuronic acid residues to AGPs, function in pollen development, polytubey block, and normal embryo development in Arabidopsis. Using biochemical and immunolabeling techniques, we demonstrated that the loss of function of the GLCAT14A, GLCAT14B, and GLCAT14C genes resulted in disorganization of the reticulate structure of the exine wall, abnormal development of the intine layer, and collapse of pollen grains in glcat14a/b and glcat14a/b/c mutants. Synchronous development between locules within the same anther was also lost in some glcat14a/b/c stamens. In addition, we observed excessive attraction of pollen tubes targeting glcat14a/b/c ovules, indicating that the polytubey block mechanism was compromised. Monosaccharide composition analysis revealed significant reductions in all sugars in glcat14a/b and glcat14a/b/c mutants except for arabinose and galactose, while immunolabeling showed decreased amounts of AGP sugar epitopes recognized by glcat14a/b and glcat14a/b/c mutants compared with the wild type. This work demonstrates the important roles that AG glucuronidation plays in Arabidopsis sexual reproduction and reproductive development.

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