LAP3, a novel plant protein required for pollen development, is essential for proper exine formation

Dobritsa, Anna A.; Nishikawa, Shuh-ichi; Preuss, Daphne; Urbańczyk-Wochniak, Ewa; Sumner, Lloyd W.; Hammond, Adam T.; Carlson, Ann L.; Swanson, Robert

doi:10.1007/s00497-009-0101-8

Cited by 65 publications

(73 citation statements)

References 67 publications

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“…Also, notably, similar proteins are absent from the genomes of early land plant lineages, such as the lycophyte Selaginella moellendorfii (spikemoss) and the bryophyte Physcomitrella patens (moss), which lack pollen but generate spores that are also covered by sporopollenin, the major component of exine. Absence of INP1 in these lineages was in contrast with the other previously described, mostly biosynthetic, exine genes-e.g., cytochromes P450 CYP704B1 and CYP703A2, MALE STERILITY2 (MS2), LESS ADHESIVE POLLEN3 (LAP3), LAP5, LAP6, ACYL-CoA SYNTHASE5 (ACOS5), NO EXINE FORMATION1 (NEF1), DEFECTIVE EXINE1 (DEX1), and THIN EXINE2 (TEX2)-all of which are present throughout the land plant lineages and some are even found in algae (Aarts et al, 1997;Paxson-Sowders et al, 2001;Ariizumi et al, 2004;Morant et al, 2007;de Azevedo Souza et al, 2009;Dobritsa et al, 2009aDobritsa et al, , 2009bDobritsa et al, , 2010Dobritsa et al, , 2011Kim et al, 2010;Chen et al, 2011;Colpitts et al, 2011). This suggests that the INP1 gene was acquired relatively recently in plant evolutionary history, after plants developed the ability to synthesize sporopollenin.…”

Section: Isolation Of the Inp1 Genementioning

confidence: 99%

The Novel Plant Protein INAPERTURATE POLLEN1 Marks Distinct Cellular Domains and Controls Formation of Apertures in the Arabidopsis Pollen Exine

2012

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Pollen grains protect the sperm cells inside them with the help of the unique cell wall, the exine, which exhibits enormous morphological variation across plant taxa, assembling into intricate and diverse species-specific patterns. How this complex extracellular structure is faithfully deposited at precise sites and acquires precise shape within a species is not understood. Here, we describe the isolation and characterization of the novel Arabidopsis thaliana gene INAPERTURATE POLLEN1 (INP1), which is specifically involved in formation of the pollen surface apertures, which arise by restriction of exine deposition at specific sites. Loss of INP1 leads to the loss of all three apertures in Arabidopsis pollen, and INP1 protein exhibits a unique tripartite localization in developing pollen, indicative of its direct involvement in specification of aperture positions. We also show that aperture length appears to be sensitive to INP1 dosage and INP1 misexpression can affect global exine patterning. Phenotypes of some inp1 mutants indicate that Arabidopsis apertures are initiated at three nonrandom positions around the pollen equator. The identification of INP1 opens up new avenues for studies of how formation of distinct cellular domains results in the production of different extracellular morphologies.

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Section: Isolation Of the Inp1 Genementioning

confidence: 99%

The Novel Plant Protein INAPERTURATE POLLEN1 Marks Distinct Cellular Domains and Controls Formation of Apertures in the Arabidopsis Pollen Exine

2012

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“…Pollen grains from the other genotypes were examined by fluorescence microscopy after staining with auramine O, a fluorescent dye that reveals exine patterns (Dobritsa et al, 2009a(Dobritsa et al, , 2009b. Fluorescence of the few tkpr1-2 mutant pollen grains that were produced ( Figure 6B) was strongly attenuated compared with the wild-type pattern ( Figure 6A), whereas only subtle alterations were seen in the exine patterns of tkpr2-1 pollen whose overall fluorescence intensity was slightly reduced ( Figure 6C).…”

Section: Disruption Of Oxidoreductase Genes Differentially Affects Pomentioning

confidence: 99%

“…Significant progress in our understanding of exine formation processes has been made recently, thanks to genetic and molecular studies of Arabidopsis mutants exhibiting defects in exine structure and deposition (Aarts et al, 1997;PaxsonSowders et al, 2001;Ariizumi et al, 2003Ariizumi et al, , 2004Ito et al, 2007;Morant et al, 2007;Yang et al, 2007;Guan et al, 2008;Suzuki et al, 2008;de Azevedo Souza et al, 2009;Dobritsa et al, 2009a;Tang et al, 2009). Unfortunately, in most cases, annotations of the mutated Arabidopsis genes found to be responsible for pollen phenotypes are primarily based on sequence similarity, and the exact functions of the corresponding proteins in pollen development remain unknown.…”

Section: Introductionmentioning

confidence: 99%

Analysis of TETRAKETIDE α-PYRONE REDUCTASE Function in Arabidopsis thaliana Reveals a Previously Unknown, but Conserved, Biochemical Pathway in Sporopollenin Monomer Biosynthesis

et al. 2010

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The precise structure of the sporopollenin polymer that is the major constituent of exine, the outer pollen wall, remains poorly understood. Recently, characterization of Arabidopsis thaliana genes and corresponding enzymes involved in exine formation has demonstrated the role of fatty acid derivatives as precursors of sporopollenin building units. Fatty acyl-CoA esters synthesized by ACYL-COA SYNTHETASE5 (ACOS5) are condensed with malonyl-CoA by POLYKETIDE SYNTHASE A (PKSA) and PKSB to yield a-pyrone polyketides required for exine formation. Here, we show that two closely related genes encoding oxidoreductases are specifically and transiently expressed in tapetal cells during microspore development in Arabidopsis anthers. Mutants compromised in expression of the reductases displayed a range of pollen exine layer defects, depending on the mutant allele. Phylogenetic studies indicated that the two reductases belong to a large reductase/ dehydrogenase gene family and cluster in two distinct clades with putative orthologs from several angiosperm lineages and the moss Physcomitrella patens. Recombinant proteins produced in bacteria reduced the carbonyl function of tetraketide a-pyrone compounds synthesized by PKSA/B, and the proteins were therefore named TETRAKETIDE a-PYRONE REDUC-TASE1 (TKPR1) and TKPR2 (previously called DRL1 and CCRL6, respectively). TKPR activities, together with those of ACOS5 and PKSA/B, identify a conserved biosynthetic pathway leading to hydroxylated a-pyrone compounds that were previously unknown to be sporopollenin precursors.

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“…Sporopollenin precursors are synthesized mainly in tapetal cells and transported to the microspore surface by the involvement of many genes in which mutations often cause strong defects in exine development. These genes include: MALE STERILITY2 (MS2) (Aarts et al, 1997), FACELESS POLLEN1 (FLP1) (Ariizumi et al, 2003), NO EXINE FORMATION1 (NEF1) (Ariizumi et al, 2004), CYP703A2 (Morant et al, 2007), ACYL-CoA SYNTHETASE5 (ACOS5) (de Azevedo Souza et al, 2009), LESS ADHERENT POLLEN3 (LAP3), LAP5/POLYKETIDE SYNTHASE B (PKSB), LAP6/POLYKETIDE SYNTHASE A (PKSA) (Dobritsa et al, 2009a;Dobritsa et al, 2010;Kim et al, 2010), CYP704B1 (Dobritsa et al, 2009b), DIHYDROFLAVONOL 4-REDUCTASE-LIKE1 (DRL1)/ TETRAKETIDEa-PYRONE REDUCTASE2 (TKPR2) (Tang et al, 2009;Grienenberger et al, 2010), TKPR1 , and a member of ATPbinding cassette transporter gene ABCG26 (Quilichini et al, 2010;Choi et al, 2011;Dou et al, 2011;Kuromori et al, 2011). Although many of these genes are specifically expressed in tapetal cells, it has been proposed that microspores also synthesize and secrete sporopollenin at the initial stage of exine development in tetrads (Wallace et al, 2011).…”

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confidence: 99%

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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LAP3, a novel plant protein required for pollen development, is essential for proper exine formation

Cited by 65 publications

References 67 publications

The Novel Plant Protein INAPERTURATE POLLEN1 Marks Distinct Cellular Domains and Controls Formation of Apertures in the Arabidopsis Pollen Exine

The Novel Plant Protein INAPERTURATE POLLEN1 Marks Distinct Cellular Domains and Controls Formation of Apertures in the Arabidopsis Pollen Exine

Analysis of TETRAKETIDE α-PYRONE REDUCTASE Function in Arabidopsis thaliana Reveals a Previously Unknown, but Conserved, Biochemical Pathway in Sporopollenin Monomer Biosynthesis

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

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