Seed mucilage evolution: Diverse molecular mechanisms generate versatile ecological functions for particular environments.
MBW master regulator
MSC toolbox genes
ecological roles
inter-species natural variability
intra-species natural variability
myxocarpy
myxodiaspory
myxospermy
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
21
03
2020
revised:
12
06
2020
accepted:
12
06
2020
pubmed:
20
6
2020
medline:
3
6
2021
entrez:
20
6
2020
Statut:
ppublish
Résumé
Plant myxodiasporous species have the ability to release a polysaccharidic mucilage upon imbibition of the seed (myxospermy) or the fruit (myxocarpy). This is a widespread capacity in angiosperms providing multiple ecological functions including higher germination efficiency under environmental stresses. It is unclear whether myxodiaspory has one or multiple evolutionary origins and why it was supposedly lost in several species. Here, we summarize recent advances on three main aspects of myxodiaspory. (a) It represents a combination of highly diverse traits at different levels of observation, ranging from the dual tissular origin of mucilage secretory cells to diverse mucilage polysaccharidic composition and ultrastructural organization. (b) An asymmetrical selection pressure is exerted on myxospermy-related genes that were first identified in Arabidopsis thaliana. The A. thaliana and the flax intra-species mucilage variants show that myxospermy is a fast-evolving trait due to high polymorphism in a few genes directly acting on mucilage establishment. In A. thaliana, these actors are downstream of a master regulatory complex and an original phylogenetic overview provided here illustrates that this complex has sequentially evolved after the common ancestor of seed plants and was fully established in the common ancestor of the rosid clade. (c) Newly identified myxodiaspory ecological functions indicate new perspectives such as soil microorganism control and plant establishment support.
Substances chimiques
Plant Mucilage
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2857-2870Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Airoldi, C. A., Hearn, T. J., Brockington, S. F., Webb, A. A. R., & Glover, B. J. (2019). TTG1 proteins regulate circadian activity as well as epidermal cell fate and pigmentation. Nature Plants, 5, 1145-1153.
Arshad, W., Sperber, K., Steinbrecher, T., Nichols, B., Jansen, V. A. A., Leubner-Metzger, G., & Mummenhoff, K. (2019). Dispersal biophysics and adaptive significance of dimorphic diaspores in the annual Aethionema arabicum (Brassicaceae). New Phytologist, 221, 1434-1446.
Arsovski, A. a., Haughn, G. W., & Western, T. L. (2010). As a model for plant cell wall research. Plant Signaling & Behavior, 5, 796-801.
Arsovski, A. A., Popma, T. M., Haughn, G. W., Carpita, N. C., McCann, M. C., & Western, T. L. (2009). AtBXL1 encodes a bifunctional -D-xylosidase/-L-arabinofuranosidase required for pectic arabinan modification in Arabidopsis mucilage secretory cells. Plant Physiology, 150, 1219-1234.
Baroux, C., & Grossniklaus, U. (2019). Seeds-An evolutionary innovation underlying reproductive success in flowering plants. Current Topics in Developmental Biology, 131, 605-642.
Barrios, D., Flores, J., González-Torres, L. R., & Palmarola, A. (2015). The role of mucilage in the germination of Leptocereus scopulophilus (Cactaceae) seeds from Pan de Matanzas, Cuba. Botany, 93, 251-255.
Basu, D., Wang, W., Ma, S., DeBrosse, T., Poirier, E., Emch, K., … Showalter, A. M. (2015). Two hydroxyproline galactosyltransferases, GALT5 and GALT2, function in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. PLoS One, 10, e0125624.
Bhatt, A., Santo, A., & Gallacher, D. (2016). Seed mucilage effect on water uptake and germination in five species from the hyper-arid Arabian desert. Journal of Arid Environments, 128, 73-79.
Chen, S., & Wang, S. (2019). GLABRA2, a common regulator for epidermal cell fate determination and anthocyanin biosynthesis in Arabidopsis. International Journal of Molecular Sciences, 20, 4997.
Chopra, D., Wolff, H., Span, J., Schellmann, S., Coupland, G., Albani, M. C., … Hülskamp, M. (2014). Analysis of TTG1 function in Arabis alpina. BMC Plant Biology, 14, 16.
Dean, G. H., Zheng, H., Tewari, J., Huang, J., Young, D. S., Hwang, Y. T., … Haughn, G. W. (2007). The Arabidopsis MUM2 gene encodes a β-galactosidase required for the production of seed coat mucilage with correct hydration properties. The Plant Cell, 19, 4007-4021.
Deng, W., Hallett, P. D., Jeng, D. S., Squire, G. R., Toorop, P. E., & Iannetta, P. P. M. (2014). The effect of natural seed coatings of Capsella bursa-pastoris L. Medik. (shepherd's purse) on soil-water retention, stability and hydraulic conductivity. Plant and Soil, 387, 167-176.
Deng, W., Jeng, D. S., Toorop, P. E., Squire, G. R., & Iannetta, P. P. M. (2012). A mathematical model of mucilage expansion in myxospermous seeds of Capsella bursa-pastoris (shepherds purse). Annals of Botany, 109, 419-427.
di Marsico, A., Scrano, L., Labella, R., Lanzotti, V., Rossi, R., Cox, L., … Amato, M. (2018). Mucilage from fruits/seeds of chia (Salvia hispanica L.) improves soil aggregate stability. Plant and Soil, 425, 57-69.
Doroshkov, A. V., Konstantinov, D. K., Afonnikov, D. A., & Gunbin, K. V. (2019). The evolution of gene regulatory networks controlling Arabidopsis thaliana L. trichome development. BMC Plant Biology, 19, 53.
Dressel, A., & Hemleben, V. (2009). Transparent Testa Glabra 1 (TTG1) and TTG1-like genes in Matthiola incana R. Br. and related Brassicaceae and mutation in the WD-40 motif. Plant Biology, 11, 204-212.
Fabrissin, I., Cueff, G., Berger, A., Granier, F., Sallé, C., Poulain, D., … North, H. M. (2019). Natural variation reveals a key role for rhamnogalacturonan I in seed outer mucilage and underlying genes. Plant Physiology, 181, 1498-1518.
Francoz, E., Ranocha, P., Burlat, V., & Dunand, C. (2015). Arabidopsis seed mucilage secretory cells: Regulation and dynamics. Trends in Plant Science, 20, 515-524.
Francoz, E., Ranocha, P., le Ru, A., Martinez, Y., Fourquaux, I., Jauneau, A., … Burlat, V. (2019). Pectin demethylesterification generates platforms that anchor peroxidases to remodel plant cell wall domains. Developmental Cell, 48, 261-276.
Galloway, A. F., Knox, P., & Krause, K. (2020). Sticky mucilages and exudates of plants: Putative microenvironmental design elements with biotechnological value. New Phytologist, 225, 1461-1469.
Galway, M. E., Masucci, J. D., Lloyd, A. M., Walbot, V., Davis, R. W., & Schiefelbein, J. W. (1994). The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Developmental Biology, 166, 740-754.
Geneve, R. L., Hildebrand, D. F., Phillips, T. D., Al-Amery, M., & Kester, S. T. (2017). Stress influences seed germination in mucilage-producing chia. Crop Science, 57, 2160-2169.
Golz, J. F., Allen, P. J., Li, S. F., Parish, R. W., Jayawardana, N. U., Bacic, A., & Doblin, M. S. (2018). Layers of regulation-Insights into the role of transcription factors controlling mucilage production in the Arabidopsis seed coat. Plant Science, 272, 179-192.
Gorai, M., el Aloui, W., Yang, X., & Neffati, M. (2014). Toward understanding the ecological role of mucilage in seed germination of a desert shrub Henophyton deserti: Interactive effects of temperature, salinity and osmotic stress. Plant and Soil, 374, 727-738.
Griffiths, J. S., & North, H. M. (2017). Sticking to cellulose: Exploiting Arabidopsis seed coat mucilage to understand cellulose biosynthesis and cell wall polysaccharide interactions. New Phytologist, 214, 959-966.
Hu, D., Baskin, J. M., Baskin, C. C., Wang, Z., Zhang, S., Yang, X., & Huang, Z. (2019). Arbuscular mycorrhizal symbiosis and achene mucilage have independent functions in seedling growth of a desert shrub. Journal of Plant Physiology, 232, 1-11.
Hu, D., Zhang, S., Baskin, J. M., Baskin, C. C., Wang, Z., Liu, R., … Huang, Z. (2019). Seed mucilage interacts with soil microbial community and physiochemical processes to affect seedling emergence on desert sand dunes. Plant Cell and Environment, 42, 591-605.
Huang, D., Wang, C., Yuan, J., Cao, J., & Lan, H. (2015). Differentiation of the seed coat and composition of the mucilage of Lepidium perfoliatum L.: A desert annual with typical myxospermy. Acta Biochimica et Biophysica Sinica, 47, 775-787.
Huang, Z., & Gutterman, Y. (1999a). Water absorption by mucilaginous achenes of Artemisia monosperma: Floating and germination as affected by salt concentrations. Israel Journal of Plant Sciences, 47, 27-34.
Huang, Z., & Gutterman, Y. (1999b). Germination of Artemisia sphaerocephala (Asteraceae), occurring in the sandy desert areas of Northwest China. South African Journal of Botany, 65, 187-196.
Jones, V. A. S., & Dolan, L. (2012). The evolution of root hairs and rhizoids. Annals of Botany, 110, 205-212.
Knee, E. M., Gong, F. C., Gao, M., Teplitski, M., Jones, A. R., Foxworthy, A., … Bauer, W. D. (2001). Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Molecular Plant-Microbe Interactions, 14, 775-784.
Kreitschitz, A., & Gorb, S. N. (2017). How does the cell wall ‘stick’ in the mucilage? A detailed microstructural analysis of the seed coat mucilaginous cell wall. Flora: Morphology, Distribution. Functional Ecology of Plants, 229, 9-22.
Kreitschitz, A., & Gorb, S. N. (2018). The micro- and nanoscale spatial architecture of the seed mucilage-Comparative study of selected plant species. PLoS One, 13, e0200522.
Kreitschitz, A., Kovalev, A., & Gorb, S. N. (2015). Slipping vs sticking: Water-dependent adhesive and frictional properties of Linum usitatissimum L. seed mucilaginous envelope and its biological significance. Acta Biomaterialia, 17, 152-159.
Kreitschitz, A., Kovalev, A., & Gorb, S. N. (2016). “Sticky invasion”-The physical properties of Plantago lanceolata L. seed mucilage. Beilstein Journal of Nanotechnology, 7, 1918-1927.
Kunieda, T., Hara-Nishimura, I., Demura, T., & Haughn, G. W. (2019). Arabidopsis FLYING SAUCER 2 functions redundantly with FLY1 to establish normal seed coat mucilage. Plant and Cell Physiology, 61, 308-317.
Kunieda, T., Mitsuda, N., Ohme-Takagi, M., Takeda, S., Aida, M., Tasaka, M., … Hara-Nishimura, I. (2008). NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. The Plant Cell, 20, 2631-2642.
Kunieda, T., Shimada, T., Kondo, M., Nishimura, M., Nishitani, K., & Hara-Nishimura, I. (2013). Spatiotemporal secretion of PEROXIDASE36 is required for seed coat mucilage extrusion in Arabidopsis. The Plant Cell, 25, 1355-1367.
Leins, P., Fligge, K., & Erbar, C. (2018). Silique valves as sails in anemochory of Lunaria (Brassicaceae). Plant Biology, 20, 238-243.
Lenser, T., Graeber, K., Cevik, Ö. S., Adigüzel, N., Dönmez, A. A., Grosche, C., … Leubner-Metzger, G. (2016). Developmental control and plasticity of fruit and seed dimorphism in Aethionema arabicum. Plant Physiology, 172, 1691-1707.
Li, C., Zhang, B., Chen, B., Ji, L., & Yu, H. (2018). Site-specific phosphorylation of TRANSPARENT TESTA GLABRA1 mediates carbon partitioning in Arabidopsis seeds. Nature Communications, 9, 571.
Li, S. F., Milliken, O. N., Pham, H., Seyit, R., Napoli, R., Preston, J., … Parish, R. W. (2009). The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. The Plant Cell, 21, 72-89.
Liu, C., Jun, J. H., & Dixon, R. A. (2014). MYB5 and MYB14 play pivotal roles in seed coat polymer biosynthesis in Medicago truncatula. Plant Physiology, 165, 1424-1439.
Liu, J., Shim, Y. Y., Shen, J., Wang, Y., Ghosh, S., & Reaney, M. J. T. (2016). Variation of composition and functional properties of gum from six Canadian flaxseed (Linum usitatissimum L.) cultivars. International Journal of Food Science and Technology, 51, 2313-2326.
Liu, K., Qi, S., Li, D., Jin, C., Gao, C., Duan, S., … Chen, M. (2017). TRANSPARENT TESTA GLABRA 1 ubiquitously regulates plant growth and development from Arabidopsis to foxtail millet (Setaria italica). Plant Science, 254, 60-69.
Liu, R., Wang, L., Tanveer, M., & Song, J. (2018). Seed heteromorphism: An important adaptation of halophytes for habitat heterogeneity. Frontiers in Plant Science, 9, 1515.
Liu, Y., Hou, H., Jiang, X., Wang, P., Dai, X., Chen, W., … Xia, T. (2018). A WD40 repeat protein from Camellia sinensis regulates anthocyanin and proanthocyanidin accumulation through the formation of MYB-bHLH-WD40 ternary complexes. International Journal of Molecular Sciences, 19, 1686.
Lloyd, A., Brockman, A., Aguirre, L., Campbell, A., Bean, A., Cantero, A., & Gonzalez, A. (2017). Advances in the MYB-bHLH-WD repeat (MBW) pigment regulatory model: Addition of a WRKY factor and co-option of an anthocyanin MYB for betalain regulation. Plant and Cell Physiology, 58, 1431-1441.
Lu, J., Tan, D., Baskin, J. M., & Baskin, C. C. (2010). Fruit and seed heteromorphism in the cold desert annual ephemeral Diptychocarpus strictus (Brassicaceae) and possible adaptive significance. Annals of Botany, 105, 999-1014.
Mabry, M., Brose, J., Blischak, P., Sutherland, B., Dismukes, W., Bottoms, C., … Pires, C. (2019). Phylogeny and multiple independent whole-genome duplication events in the Brassicales. bioRxiv Preprint.
Macquet, A., Ralet, M. C., Kronenberger, J., Marion-Poll, A., & North, H. M. (2007). In situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. Plant and Cell Physiology, 48, 984-999.
Macquet, A., Ralet, M.-C., Loudet, O., Kronenberger, J., Mouille, G., Marion-Poll, A., & North, H. M. (2007). A naturally occurring mutation in an Arabidopsis accession affects a β-d-galactosidase that increases the hydrophilic potential of rhamnogalacturonan I in seed mucilage. The Plant Cell, 19, 3990-4006.
Matsui, K., Hiratsu, K., Koyama, T., Tanaka, H., & Ohme-Takagi, M. (2005). A chimeric AtMYB23 repressor induces hairy roots, elongation of leaves and stems, and inhibition of the deposition of mucilage on seed coats in Arabidopsis. Plant and Cell Physiology, 46, 147-155.
Meschke, H., & Schrempf, H. (2010). Streptomyces lividans inhibits the proliferation of the fungus Verticillium dahliae on seeds and roots of Arabidopsis thaliana. Microbial Biotechnology, 3, 428-443.
Miart, F., Fournet, F., Dubrulle, N., Petit, E., Demailly, H., Dupont, L., … Pageau, K. (2019). Cytological approaches combined with chemical analysis reveals the layered nature of flax mucilage. Frontiers in Plant Science, 10, 684.
Mirhosseini, H., & Amid, B. T. (2012). A review study on chemical composition and molecular structure of newly plant gum exudates and seed gums. Food Research International, 46, 387-398.
Nguyen, C. T., Tran, G. B., & Nguyen, N. H. (2019). The MYB-bHLH-WDR interferers (MBWi) epigenetically suppress the MBW's targets. Biology of the Cell, 111, 284-291.
North, H. M., Berger, A., Saez-Aguayo, S., & Ralet, M. C. (2014). Understanding polysaccharide production and properties using seed coat mutants: Future perspectives for the exploitation of natural variants. Annals of Botany, 114, 1251-1263.
Pang, Y., Wenger, J. P., Saathoff, K., Peel, G. J., Wen, J., Huhman, D., … Dixon, R. A. (2009). A WD40 repeat protein from Medicago truncatula is necessary for tissue-specific anthocyanin and proanthocyanidin biosynthesis but not for trichome development. Plant Physiology, 151, 1114-1129.
Penfield, S. (2001). MYB61 is required for mucilage deposition and extrusion in the Arabidopsis seed coat. The Plant Cell, 13, 2777-2791.
Phan, J. L., & Burton, R. A. (2018). New insights into the composition and structure of seed mucilage. In Annual plant reviews (pp. 1-41). Chichester, England: John Wiley & Sons.
Poulain, D., Botran, L., North, H. M., & Ralet, M.-C. (2019). Composition and physicochemical properties of outer mucilage from seeds of Arabidopsis natural accessions. AoB Plants, 11, plz031.
Rautengarten, C., Usadel, B., Neumetzler, L., Hartmann, J., Büssis, D., & Altmann, T. (2008). A subtilisin-like serine protease essential for mucilage release from Arabidopsis seed coats. Plant Journal, 54, 466-480.
Raviv, B., Aghajanyan, L., Granot, G., Makover, V., Frenkel, O., Gutterman, Y., & Grafi, G. (2017). The dead seed coat functions as a long-term storage for active hydrolytic enzymes. PLoS One, 12, e0181102.
Renzaglia, K. S., Duff, R. J., Nickrent, D. L., & Garbary, D. J. (2000). Vegetative and reproductive innovations of early land plants: Implications for a unified phylogeny. Philosophical Transactions of the Royal Society B: Biological Sciences, 355, 769-793.
Roberts, H. R., Warren, J. M., & Provan, J. (2018). Evidence for facultative protocarnivory in Capsella bursa-pastoris seeds. Scientific Reports, 8, 10120.
Ryding, O. (2001). Myxocarpy in the nepetoideae (Lamiaceae) with notes on myxodiaspory in general. Systematics and Geography of Plants, 71, 503-514.
Saez-Aguayo, S., Ralet, M.-C., Berger, A., Botran, L., Ropartz, D., Marion-Poll, A., & North, H. M. (2013). PECTIN METHYLESTERASE INHIBITOR6 promotes Arabidopsis mucilage release by limiting methylesterification of homogalacturonan in seed coat epidermal cells. The Plant Cell, 25, 308-323.
Saez-Aguayo, S., Rondeau-Mouro, C., Macquet, A., Kronholm, I., Ralet, M. C., Berger, A., … North, H. M. (2014). Local evolution of seed flotation in Arabidopsis. PLoS Genetics, 10, e1004221.
Shimada, T., Kunieda, T., Sumi, S., Koumoto, Y., Tamura, K., Hatano, K., … Hara-Nishimura, I. (2018). The AP-1 complex is required for proper mucilage formation in Arabidopsis seeds. Plant & Cell Physiology, 59, 2331-2338.
Šola, K., Dean, G. H., & Haughn, G. W. (2019). Arabidopsis seed mucilage: A specialised extracellular matrix that demonstrates the structure-function versatility of cell wall polysaccharides. In Annual plant reviews online, 2, (pp. 1085-1116). New Jersey, USA: Wiley Online Library.
Šola, K., Gilchrist, E. J., Ropartz, D., Wang, L., Feussner, I., Mansfield, S. D., … Haughn, G. W. (2019). RUBY, a putative galactose oxidase, influences pectin properties and promotes cell-to-cell adhesion in the seed coat epidermis of Arabidopsis. The Plant Cell, 31, 809-831.
Song, Y., He, L., Wang, X.-D., Smith, N., Wheeler, S., Garg, M. L., & Rose, R. J. (2017). Regulation of carbon partitioning in the seed of the model legume Medicago truncatula and Medicago orbicularis: A comparative approach. Frontiers in Plant Science, 8, 2070.
Soto-Cerda, B. J., Cloutier, S., Quian, R., Gajardo, H. A., Olivos, M., & You, F. M. (2018). Genome-wide association analysis of mucilage and hull content in flax (Linum usitatissimum l.) seeds. International Journal of Molecular Sciences, 19, 2870.
Soukoulis, C., Gaiani, C., & Hoffmann, L. (2018). Plant seed mucilage as emerging biopolymer in food industry applications. Current Opinion in Food Science, 22, 28-42.
Sullivan, A. M., Arsovski, A. A., Thompson, A., Sandstrom, R., Thurman, R. E., Neph, S., … Queitsch, C. (2019). Mapping and dynamics of regulatory DNA in maturing Arabidopsis thaliana siliques. Frontiers in Plant Science, 10, 1434.
Takenaka, Y., Kato, K., Ogawa-Ohnishi, M., Tsuruhama, K., Kajiura, H., Yagyu, K., … Ishimizu, T. (2018). Pectin RG-I rhamnosyltransferases represent a novel plant-specific glycosyltransferase family. Nature Plants, 4, 669-676.
Toorop, P. E., Campos Cuerva, R., Begg, G. S., Locardi, B., Squire, G. R., & Iannetta, P. P. M. (2012). Co-adaptation of seed dormancy and flowering time in the arable weed Capsella bursa-pastoris (shepherds purse). Annals of Botany, 109, 481-489.
Tsai, A. Y. L., Higaki, T., Nguyen, C. N., Perfus-Barbeoch, L., Favery, B., & Sawa, S. (2019). Regulation of root-knot nematode behavior by seed-coat mucilage-derived attractants. Molecular Plant, 12, 99-112.
Tucker, M. R., Ma, C., Phan, J., Neumann, K., Shirley, N. J., Hahn, M. G., … Burton, R. A. (2017). Dissecting the genetic basis for seed coat mucilage heteroxylan biosynthesis in Plantago ovata using gamma irradiation and infrared spectroscopy. Frontiers in Plant Science, 8, 328.
Usadel, B. (2004). RHM2 is involved in mucilage pectin synthesis and is required for the development of the seed coat in Arabidopsis. Plant Physiology, 134, 286-295.
van Wijk, R., Zhang, Q., Zarza, X., Lamers, M., Marquez, F. R., Guardia, A., … Munnik, T. (2018). Role for Arabidopsis PLC7 in stomatal movement, seed mucilage attachment, and leaf serration. Frontiers in Plant Science, 9, 1721.
Vaughan, J. G., & Whitehouse, J. M. (1971). Seed structure and the taxonomy of the Cruciferae. Botanical Journal of the Linnean Society, 64, 383-409.
Voiniciuc, C., Engle, K. A., Günl, M., Dieluweit, S., Schmidt, M. H.-W., Yang, J.-Y., … Usadel, B. (2018). Identification of key enzymes for pectin synthesis in seed mucilage. Plant Physiology, 178, 1045-1064.
Voiniciuc, C., Yang, B., Schmidt, M. H. W., Günl, M., & Usadel, B. (2015). Starting to gel: How Arabidopsis seed coat epidermal cells produce specialized secondary cell walls. International Journal of Molecular Sciences, 16, 3452-3473.
Voiniciuc, C., Zimmermann, E., Schmidt, M. H.-W., Günl, M., Fu, L., North, H. M., & Usadel, B. (2016). Extensive natural variation in Arabidopsis seed mucilage structure. Frontiers in Plant Science, 7, 803.
Walker, A. R., Davison, P. A., Bolognesi-Winfield, A. C., James, C. M., Srinivasan, N., Blundell, T. L., … Gray, J. C. (1999). The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. The Plant Cell, 11, 1337-1349.
Wang, M., Xu, Z., Ahmed, R. I., Wang, Y., Hu, R., Zhou, G., & Kong, Y. (2019). Tubby-like protein 2 regulates homogalacturonan biosynthesis in Arabidopsis seed coat mucilage. Plant Molecular Biology, 99, 421-436.
Weitbrecht, K., Müller, K., & Leubner-Metzger, G. (2011). First off the mark: Early seed germination. Journal of Experimental Botany, 62, 3289-3309.
Western, T. L. (2001). Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiology, 127, 998-1011.
Western, T. L. (2012). The sticky tale of seed coat mucilages: Production, genetics, and role in seed germination and dispersal. Seed Science Research, 22, 1-25.
Witztum, A., Gutterman, Y., & Evenari, M. (1969). Integumentary mucilage as an oxygen barrier during germination of Blepharis persica. Botanical Gazette, 130, 238-241.
Xu, W., Dubos, C., & Lepiniec, L. (2015). Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends in Plant Science, 20, 176-185.
Yang, B., Voiniciuc, C., Fu, L., Dieluweit, S., Klose, H., & Usadel, B. (2019). TRM4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA3. New Phytologist, 221, 881-895.
Yang, X., Baskin, C. C., Baskin, J. M., Liu, G., & Huang, Z. (2012). Seed mucilage improves seedling emergence of a sand desert shrub. PLoS One, 7, e34897.
Yang, X., Baskin, C. C., Baskin, J. M., Zhang, W., & Huang, Z. (2012). Degradation of seed mucilage by soil microflora promotes early seedling growth of a desert sand dune plant. Plant, Cell and Environment, 35, 872-883.
Yang, X., Baskin, J. M., Baskin, C. C., & Huang, Z. (2012). More than just a coating: Ecological importance, taxonomic occurrence and phylogenetic relationships of seed coat mucilage. Perspectives in Plant Ecology, Evolution and Systematics, 14, 434-442.
Yu, L., Lyczakowski, J. J., Pereira, C. S., Kotake, T., Yu, X., Li, A., … Dupree, P. (2018). The patterned structure of galactoglucomannan suggests it may bind to cellulose in seed mucilage. Plant Physiology, 178, 1011-1026.
Yu, L., Yakubov, G. E., Zeng, W., Xing, X., Stenson, J., Bulone, V., & Stokes, J. R. (2017). Multi-layer mucilage of Plantago ovata seeds: Rheological differences arise from variations in arabinoxylan side chains. Carbohydrate Polymers, 165, 132-141.
Zhang, B., Chopra, D., Schrader, A., & Hülskamp, M. (2019). Evolutionary comparison of competitive protein-complex formation of MYB, bHLH, and WDR proteins in plants. Journal of Experimental Botany, 70, 3197-3209.
Zhang, B., & Hülskamp, M. (2019). Evolutionary analysis of MBW function by phenotypic Rescue in Arabidopsis thaliana. Frontiers in Plant Science, 10, 375.