A Large-Scale Genetic Screen in Arabidopsis to Identify Genes Involved in Pollen Exine Production

Dobritsa, Anna A.; Geanconteri, Aliza; Shrestha, Jay; Carlson, Ann L.; Kooyers, Nicholas J.; Coerper, Daniel; Urbańczyk-Wochniak, Ewa; Bench, Bennie J.; Sumner, Lloyd W.; Swanson, Robert; Preuss, Daphney

doi:10.1104/pp.111.179523

Cited by 125 publications

(159 citation statements)

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“…In this article, we focus on a unique type-2 mutant, kns4, in which the exine is less than half the thickness of wild type but still has a reticulate structure. Another characteristic of kns4 is that mature pollen grains of the mutant often aggregate .A similar genetic screen was carried out by Dobritsa et al, (2011) with an Arabidopsis T-DNA insertion population and many mutants with a variety of defects in exine structure were found. For example, the exine of spongy2 (spg2) has irregularly distributed and elongated tectum elements and lacunae (holes within the tectum) of variable size and shape.…”

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“…For example, the exine of spongy2 (spg2) has irregularly distributed and elongated tectum elements and lacunae (holes within the tectum) of variable size and shape. Another mutant, uneven pattern of exine1 (upex1), shows a grossly disorganized exine (Dobritsa et al, 2011). Only part of the upex1 pollen surface maintains a reticulate structure; other areas either lack exine or have essentially smooth exine with small lacunae (Dobritsa et al, 2011).…”

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KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

et al. 2016

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Pollen exine is essential for protection from the environment of the male gametes of seed-producing plants, but its assembly and composition remain poorly understood. We previously characterized Arabidopsis (Arabidopsis thaliana) mutants with abnormal pollen exine structure and morphology that we named kaonashi (kns). Here we describe the identification of the causal gene of kns4 that was found to be a member of the CAZy glycosyltransferase 31 gene family, identical to UNEVEN PATTERN OF EXINE1, and the biochemical characterization of the encoded protein. The characteristic exine phenotype in the kns4 mutant is related to an abnormality of the primexine matrix laid on the surface of developing microspores. Using light microscopy with a combination of type II arabinogalactan (AG) antibodies and staining with the arabinogalactan-protein (AGP)-specific b-Glc Yariv reagent, we show that the levels of AGPs in the kns4 microspore primexine are considerably diminished, and their location differs from that of wild type, as does the distribution of pectin labeling. Furthermore, kns4 mutants exhibit reduced fertility as indicated by shorter fruit lengths and lower seed set compared to the wild type, confirming that KNS4 is critical for pollen viability and development. KNS4 was heterologously expressed in Nicotiana benthamiana, and was shown to possess b-(1,3)-galactosyltransferase activity responsible for the synthesis of AG glycans that are present on both AGPs and/or the pectic polysaccharide rhamnogalacturonan I. These data demonstrate that defects in AGP/pectic glycans, caused by disruption of KNS4 function, impact pollen development and viability in Arabidopsis.Pollen, the male gametophyte of all seed plants, is crucial for reproductive success. Due to the harsh environmental conditions that pollen must survive in, it has developed an elaborate and specialized cell wall. However, despite its importance our knowledge of the fine structure and assembly of the pollen grain wall is poorly understood (Newbigin et al., 2009;Ariizumi and Toriyama, 2011;Quilichini et al., 2015;Shi et al., 2015). Arabidopsis (Arabidopsis thaliana) provides an ideal genetic and cell biological model to dissect the assembly of the components of the pollen grain wall. Arabidopsis pollen grains have a typical surface structure that consists of an inner intine layer, which is usually made up of cellulose and pectin, and the outer exine, which is largely composed of sporopollenin (Li et al., 1995). The exine is further subdivided into inner nexine and outer sexine. The sexine has a three-dimensional (3D) structure composed of many columns called baculae and a roof called tectum. These two structures give the Arabidopsis pollen surface a reticulate appearance with a uniform mesh size. The nexine is composed of outer nexine I (foot layer), which contains sporopollenin, and inner nexine II (endexine; Ariizumi and Toriyama, 2011;Jiang et al., 2013). A recent study suggests that arabinogalactan proteins (AGPs) are key constituents of nexine with express...

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KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

et al. 2016

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“…The initial binding of compatible A. thaliana pollen to the stigmatic papilla was determined to be mediated by the pollen exine , while the pollen coat was not required (Zinkl et al 1999 ). Consistent with this, a genetic screen for mutants disrupted in this initial adhesion stage resulted in a number of mutants with exine defects (Nishikawa et al 2005 ;Dobritsa et al 2011 ). The pollen coat is then involved in further adhesion of the pollen grain to the stigmatic papilla.…”

Section: Pollen-stigma Components For Compatible Pollen Acceptancementioning

confidence: 88%

Signaling Events in Pollen Acceptance or Rejection in the Arabidopsis Species

Indriolo

Safavian

Goring

2014

Sexual Reproduction in Animals and Plants

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The initial events of pollen-pistil interactions are fundamentally important in fl owering plants because they infl uence successful fertilization. These early events include the recognition of pollen grains through signaling events in the pistil that will lead to the acceptance of a compatible pollen grain or the rejection of an incompatible pollen grain. There has been much research into this fi eld in the Brassicaceae, as this family includes many agriculturally important crops such as canola, radish, turnip, and cabbage. However, this review focuses on what is known about the early pollen-pistil interactions in the experimentally tractable Arabidopsis genus, including Arabidopsis thaliana (a self-compatible species) and Arabidopsis lyrata (a self-incompatible species). Compatible pollinations are driven by the ability of the pistil to provide the resources for an acceptable pollen grain to hydrate, germinate, and fertilize the ovule. Self-incompatible species have a receptorligand signaling pathway that rejects self-pollen grains, preventing inbreeding and encouraging genetic diversity within the species. There is some overlap between these two pathways, and current research is looking for unknown elements and downstream events following the initial recognition of a pollen grain in Arabidopsis .

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“…Recent identification of the involvement of GPI-anchored nonspecific lipid transfer proteins in the biosynthesis or deposition of sporopollenin (Edstam et al, 2013) might suggest the role of Dol, a compulsory cofactor of the biosynthesis of GPI-anchored proteins, in sporopollenin biosynthesis. Despite the observations described above, genes encoding proteins of the Dol cycle, e.g., CPT, DOK, and PPRD, escaped identification within a large-scale genetic screen aimed at detection of those involved in pollen exine production (Suzuki et al, 2008;Dobritsa et al, 2011).…”

Section: Polyprenol Reductase: a Regulator Of Pollen Developmentmentioning

confidence: 99%

POLYPRENOL REDUCTASE2 Deficiency Is Lethal in Arabidopsis Due to Male Sterility

et al. 2015

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Dolichol is a required cofactor for protein glycosylation, the most common posttranslational modification modulating the stability and biological activity of proteins in all eukaryotic cells. We have identified and characterized two genes, PPRD1 and -2, which are orthologous to human SRD5A3 (steroid 5a reductase type 3) and encode polyprenol reductases responsible for conversion of polyprenol to dolichol in Arabidopsis thaliana. PPRD1 and -2 play dedicated roles in plant metabolism. PPRD2 is essential for plant viability; its deficiency results in aberrant development of the male gametophyte and sporophyte. Impaired protein glycosylation seems to be the major factor underlying these defects although disturbances in other cellular dolicholdependent processes could also contribute. Shortage of dolichol in PPRD2-deficient cells is partially rescued by PPRD1 overexpression or by supplementation with dolichol. The latter has been discussed as a method to compensate for deficiency in protein glycosylation. Supplementation of the human diet with dolichol-enriched plant tissues could allow new therapeutic interventions in glycosylation disorders. This identification of PPRD1 and -2 elucidates the factors mediating the key step of the dolichol cycle in plant cells which makes manipulation of dolichol content in plant tissues feasible.

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A Large-Scale Genetic Screen in Arabidopsis to Identify Genes Involved in Pollen Exine Production

Cited by 125 publications

References 107 publications

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

Signaling Events in Pollen Acceptance or Rejection in the Arabidopsis Species

POLYPRENOL REDUCTASE2 Deficiency Is Lethal in Arabidopsis Due to Male Sterility

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