The hydroxyproline O-arabinosyltransferase FIN4 is required for tomato pollen intine development.
Cell wall
Glycosylation
Hydration
Intine
Pollen
Journal
Plant reproduction
ISSN: 2194-7961
Titre abrégé: Plant Reprod
Pays: Germany
ID NLM: 101602701
Informations de publication
Date de publication:
Jun 2023
Jun 2023
Historique:
received:
03
11
2022
accepted:
20
01
2023
medline:
12
6
2023
pubmed:
8
2
2023
entrez:
7
2
2023
Statut:
ppublish
Résumé
The pollen grain cell wall is a highly specialized structure composed of distinct layers formed through complex developmental pathways. The production of the innermost intine layer, composed of cellulose, pectin and other polymers, is particularly poorly understood. Here we demonstrate an important and specific role for the hydroxyproline O-arabinosyltransferase (HPAT) FIN4 in tomato intine development. HPATs are plant-specific enzymes which initiate glycosylation of certain cell wall structural proteins and signaling peptides. FIN4 was expressed throughout pollen development in both the developing pollen and surrounding tapetal cells. A fin4 mutant with a partial deletion of the catalytic domain displayed significantly reduced male fertility in vivo and compromised pollen hydration and germination in vitro. However, fin4 pollen that successfully germinated formed morphologically normal pollen tubes with the same growth rate as the wild-type pollen. When we examined mature fin4 pollen, we found they were cytologically normal, and formed morphologically normal exine, but produced significantly thinner intine. During intine deposition at the late stages of pollen development we found fin4 pollen had altered polymer deposition, including reduced cellulose and increased detection of pectin, specifically homogalacturonan with both low and high degrees of methylesterification. Therefore, FIN4 plays an important role in intine formation and, in turn pollen hydration and germination and the process of intine formation involves dynamic changes in the developing pollen cell wall.
Identifiants
pubmed: 36749417
doi: 10.1007/s00497-023-00459-6
pii: 10.1007/s00497-023-00459-6
doi:
Substances chimiques
arabinosyltransferase
EC 2.4.2.-
Hydroxyproline
RMB44WO89X
Pectins
89NA02M4RX
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
173-191Subventions
Organisme : Division of Integrative Organismal Systems
ID : IOS-1755482
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Beuder S, Dorchak A, Bhide A, Moeller SR, Petersen BL, MacAlister CA (2020) Exocyst mutants suppress pollen tube growth and cell wall structural defects of hydroxyproline O-arabinosyltransferase mutants. Plant J 103(4):1399–1419. https://doi.org/10.1111/tpj.14808
doi: 10.1111/tpj.14808
pubmed: 32391581
pmcid: 7496944
Beuder S, Lara-Mondragón C, Dorchak A, MacAlister CA (2022) SEC1A is a major Arabidopsis Sec1/Munc18 gene in vesicle trafficking during pollen tube tip growth. Plant J 110(5):1353–1369
doi: 10.1111/tpj.15742
pubmed: 35306707
pmcid: 9322465
Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174(3):483–498. https://doi.org/10.1111/j.1469-8137.2007.02060.x
doi: 10.1111/j.1469-8137.2007.02060.x
pubmed: 17447905
Borassi C, Sede AR, Mecchia MA, Salgado Salter JD, Marzol E, Muschietti JP, Estevez JM (2016) An update on cell surface proteins containing extensin-motifs. J Exp Bot 67(2):477–487. https://doi.org/10.1093/jxb/erv455
doi: 10.1093/jxb/erv455
pubmed: 26475923
Brodie R, Roper RL, Upton C (2004) JDotter: a Java interface to multiple dotplots generated by dotter. Bioinformatics 20(2):279–281. https://doi.org/10.1093/bioinformatics/btg406
doi: 10.1093/bioinformatics/btg406
pubmed: 14734323
Brooks C, Nekrasov V, Lipppman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166(3):1292–1297. https://doi.org/10.1104/pp.114.247577
doi: 10.1104/pp.114.247577
pubmed: 25225186
pmcid: 4226363
Cankar K, Kortstee A, Toonen MAJ, Wolters-Arts M, Houbein R, Mariani C, Ulvskov P, Jorgensen B, Schols HA, Visser RGF, Trindade LM (2014) Pectic arabinan side chains are essential for pollen cell wall integrity during pollen development. Plant Biotechnol J 12(4):492–502. https://doi.org/10.1111/pbi.12156
doi: 10.1111/pbi.12156
pubmed: 24428422
Cannon MC, Terneus K, Hall Q, Tan L, Wang Y, Wegenhart BL, Chen L, Lamport DTAA, Chen Y, Kieliszewski MJ (2008) Self-assembly of the plant cell wall requires an extensin scaffold. Proc Natl Acad Sci USA 105(6):2226–2231. https://doi.org/10.1073/pnas.0711980105
doi: 10.1073/pnas.0711980105
pubmed: 18256186
pmcid: 2538902
Carvalho RF, Campos ML, Pino LE, Crestana SL, Zsögön A, Lima JE, Benedito VA, Peres LEP (2011) Convergence of developmental mutants into a single tomato model system: “Micro-Tom” as an effective toolkit for plant development research. Plant Methods 7(1):1–14. https://doi.org/10.1186/1746-4811-7-18
doi: 10.1186/1746-4811-7-18
Cascallares M, Setzes N, Marchetti F, López JA, Distéfano AM, Cainzos M, Zabaleta E, Pagnussat GC (2020) A complex journey: Cell wall remodeling, interactions, and integrity during pollen tube growth. Front Plant Sci 11:599247. https://doi.org/10.3389/fpls.2020.599247
doi: 10.3389/fpls.2020.599247
pubmed: 33329663
pmcid: 7733995
Chebli Y, Kaneda M, Zerzour R, Geitmann A (2012) The cell wall of the Arabidopsis pollen tube-spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160(4):1940–1955. https://doi.org/10.1104/pp.112.199729
doi: 10.1104/pp.112.199729
pubmed: 23037507
pmcid: 3510122
Chen Y, Dong W, Tan L, Held MA, Kieliszewski MJ (2015) Arabinosylation plays a crucial role in extensin cross-linking in vitro. Biochem Insights 8(Supple 2):1–13. https://doi.org/10.4137/BCI.S31353
doi: 10.4137/BCI.S31353
pubmed: 26568683
pmcid: 4629521
Choudhary P, Saha P, Ray T, Tang Y, Yang D, Cannon MC (2015) EXTENSIN18 is required for full male fertility as well as normal vegetative growth in Arabidopsis. Front Plant Sci 6(JULY):1–14. https://doi.org/10.3389/fpls.2015.00553
doi: 10.3389/fpls.2015.00553
Christiaens S, Van Buggenhout S, Ngouémazong ED, Vandevenne E, Fraeye I, Duvetter T, Van Loey AM, Hendrickx ME (2011) Anti-homogalacturonan antibodies: a way to explore the effect of processing on pectin in fruits and vegetables? Food Res Int 44(1):225–234. https://doi.org/10.1016/j.foodres.2010.10.031
doi: 10.1016/j.foodres.2010.10.031
Ding Q, Yan X, Pi Y, Li Z, Xue J, Chen H, Li Y, Wu H (2020) Genome-wide identification and expression analysis of extensin genes in tomato. Genomics 112(6):4348–4360. https://doi.org/10.1016/j.ygeno.2020.07.029
doi: 10.1016/j.ygeno.2020.07.029
pubmed: 32712296
Dobritsa AA, Geanconteri A, Shrestha J, Carlson A, Kooyers N, Coerper D, Urbanczyk-wochniak E, Bench BJ, Sumner LW, Swanson R, Preuss D (2011) A large-scale genetic screen in Arabidopsis to identify genes involved in pollen exine production. Plant Physiol 157(2):947–970. https://doi.org/10.1104/pp.111.179523
doi: 10.1104/pp.111.179523
pubmed: 21849515
pmcid: 3192556
Drakakaki G, Zabotina O, Delgado I, Stephanie R, Keegstra K, Raikhel N (2006) Arabidopsis reversibly glycosylated polypeptides 1 and 2 are essential for pollen development. Plant Physiol 142:1480–1492. https://doi.org/10.1104/pp.106.086363
doi: 10.1104/pp.106.086363
pubmed: 17071651
pmcid: 1676068
Dresselhaus T, Franklin-Tong N (2013) Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6(4):1018–1036. https://doi.org/10.1093/mp/sst061
doi: 10.1093/mp/sst061
pubmed: 23571489
Egelund J, Obel N, Ulvskov P, Geshi N, Pauly M, Bacic A, Petersen BL (2007) Molecular characterization of two Arabidopsis thaliana glycosyltransferase mutants rra1 and rra2 which have a reduced residual arabinose content in a polymer tightly associated with the cellulosic wall residue. Plant Mol Biol 64(4):439–451. https://doi.org/10.1007/s11103-007-9162-y
doi: 10.1007/s11103-007-9162-y
pubmed: 17401635
Fabrice TN, Vogler H, Draeger C, Munglani G, Gupta S, Herger AG, Knox P, Grossniklaus U, Ringli C (2018) LRX Proteins play a crucial role in pollen grain and pollen tube cell wall development. Plant Physiol 176(3):1981–1992. https://doi.org/10.1104/pp.17.01374
doi: 10.1104/pp.17.01374
pubmed: 29247121
Fan T, Park S, Shi Q, Zhang X, Liu Q, Song Y, Chin H, Ibrahim MSB, Mokrzecka N, Yang Y, Li H, Song J, Suresh S (2020) Transformation of hard pollen into soft matter. Nat Commun 11(1):1449. https://doi.org/10.1038/s41467-020-15294-w
doi: 10.1038/s41467-020-15294-w
pubmed: 32193375
pmcid: 7081183
Fang K, Wang Y, Yu T, Zhang L, Baluška F, Šamaj J, Lin J (2008) Isolation of de-exined pollen and cytological studies of the pollen intines of Pinus bungeana Zucc. Ex Endl. and Picea wilsonii Mast. Flora: Morphol Distrib Funct Ecol Plants 203(4):332–340. https://doi.org/10.1016/j.flora.2007.04.007
doi: 10.1016/j.flora.2007.04.007
Fernandez-Pozo N, Menda N, Edwards JD, Saha S, Tecle IY, Strickler SR, Bombarely A, Fisher-York T, Pujar A, Foerster H, Yan A, Mueller LA (2015) The Sol Genomics Network (SGN)-from genotype to phenotype to breeding. Nucleic Acids Res 43(D1):D1036–D1041. https://doi.org/10.1093/nar/gku1195
doi: 10.1093/nar/gku1195
pubmed: 25428362
Gille S, Hänsel U, Ziemann M, Pauly M (2009) Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases. Proc Natl Acad Sci 106(34):14699–14704. https://doi.org/10.1073/pnas.0905434106
doi: 10.1073/pnas.0905434106
pubmed: 19667208
pmcid: 2731844
Giorno F, Wolters-Arts M, Mariani C, Rieu I (2013) Ensuring reproduction at high temperatures: the heat stress response during anther and pollen development. Plants 2(3):489–506. https://doi.org/10.3390/plants2030489
doi: 10.3390/plants2030489
pubmed: 27137389
pmcid: 4844380
Grienenberger E, Quilichini TD (2021) The toughest material in the plant kingdom: an update on sporopollenin. Front Plant Sci 12:703864. https://doi.org/10.3389/fpls.2021.703864
doi: 10.3389/fpls.2021.703864
pubmed: 34539697
pmcid: 8446667
Haas TT, Wightman R, Peaucelle A, Höfte H (2021) The role of pectin phase separation in plant cell wall assembly and growth. Cell Surf. 7:100054. https://doi.org/10.1016/j.tcsw.2021.100054
doi: 10.1016/j.tcsw.2021.100054
pubmed: 34141960
pmcid: 8185244
Hackenberg D, Twell D (2019) The evolution and patterning of male gametophyte development. Curr Top Dev Biol 131:257–298. https://doi.org/10.1016/bs.ctdb.2018.10.008
doi: 10.1016/bs.ctdb.2018.10.008
pubmed: 30612620
Held MA, Tan L, Kamyab A, Hare M, Shpak E, Kieliszewski MJ (2004) Di-isodityrosine is the intermolecular cross-link of isodityrosine-rich extensin analogs cross-linked in vitro. J Biol Chem 279(53):55474–55482. https://doi.org/10.1074/jbc.M408396200
doi: 10.1074/jbc.M408396200
pubmed: 15465824
Herburger K, Holzinger A (2016) Aniline blue and calcofluor white staining of callose and cellulose in the streptophyte green algae zygnema and klebsormidium. Bio-Protoc 6(20):6–10. https://doi.org/10.21769/bioprotoc.1969
doi: 10.21769/bioprotoc.1969
Heslop-Harrison J (1968) Pollen wall development. Science 161(3838):230–237. https://doi.org/10.1126/science.161.3838.230
doi: 10.1126/science.161.3838.230
pubmed: 5657325
Hess MW (1993) Cell-wall development in freeze-fixed pollen: Intine formation of Ledebouria socialis (Hyacinthaceae). Planta 189(1):139–149. https://doi.org/10.1007/BF00201354
doi: 10.1007/BF00201354
Hess MW, Frosch A (1994) Subunits of forming pollen exine and Ubisch bodies as seen in freeze substituted Ledebouria socialis Roth (Hyacinthaceae). Protoplasma 182(1–2):10–14. https://doi.org/10.1007/BF01403683
doi: 10.1007/BF01403683
Jaffri SRF, Macalister CA (2021) Sequential deposition and remodeling of cell wall polymers during tomato pollen development. Front Plant Sci 12:703713. https://doi.org/10.3389/fpls.2021.703713
doi: 10.3389/fpls.2021.703713
pubmed: 34386029
pmcid: 8354551
Jahnen W, Lush WM, Clarke AE (1989) Inhibition of in vitro pollen tube growth by isolated S-glycoproteins of Nicotiana alata. Plant Cell 1(5):501. https://doi.org/10.2307/3868970
doi: 10.2307/3868970
pubmed: 12359898
pmcid: 159783
Javelle M, Marco CF, Timmermans M (2011) In situ hybridization for the precise localization of transcripts in plants. J vis Exp 57:1–10. https://doi.org/10.3791/3328
doi: 10.3791/3328
Jiang J, Zhang Z, Cao J (2013) Pollen wall development: the associated enzymes and metabolic pathways. Plant Biol 15(2):249–263. https://doi.org/10.1111/j.1438-8677.2012.00706.x
doi: 10.1111/j.1438-8677.2012.00706.x
pubmed: 23252839
Jiang J, Yao L, Yu Y, Liang Y, Jiang J, Ye N, Miao Y, Cao J (2014a) PECTATE LYASE-LIKE 9 from Brassica campestris is associated with intine formation. Plant Sci 229:66–75. https://doi.org/10.1016/j.plantsci.2014.08.008
doi: 10.1016/j.plantsci.2014.08.008
pubmed: 25443834
Jiang J, Yao L, Yu Y, Lv M, Miao Y, Cao J (2014b) PECTATE LYASE-LIKE10 is associated with pollen wall development in Brassica campestris. J Integr Plant Biol 56(11):1095–1105. https://doi.org/10.1111/jipb.12209
doi: 10.1111/jipb.12209
pubmed: 24773757
Kaur D, Moreira D, Coimbra S, Showalter AM (2022) Hydroxyproline-O-Galactosyltransferases synthesizing type II arabinogalactans are essential for male gametophytic development in Arabidopsis. Front Plant Sci 13:935413. https://doi.org/10.3389/fpls.2022.935413
doi: 10.3389/fpls.2022.935413
pubmed: 35774810
pmcid: 9237623
Kotake T, Yamanashi Y, Imaizumi C, Tsumuraya Y (2016) Metabolism of L-arabinose in plants. J Plant Res 129(5):781–792. https://doi.org/10.1007/s10265-016-0834-z
doi: 10.1007/s10265-016-0834-z
pubmed: 27220955
pmcid: 5897480
Kudo T, Kobayashi M, Terashima S, Katayama M, Ozaki S, Kanno M, Saito M, Yokoyama K, Ohyanagi H, Aoki K, Kubo Y, Yano K (2017) TOMATOMICS: A web database for integrated omics information in tomato. Plant Cell Physiol 58(1):e8. https://doi.org/10.1093/pcp/pcw207
doi: 10.1093/pcp/pcw207
pubmed: 28111364
pmcid: 5444566
Lamport DTA, Miller DH (1971) Hydroxyproline arabinosides in the plant kingdom. Plant Physiol 48(4):454–456. https://doi.org/10.1104/pp.48.4.454
doi: 10.1104/pp.48.4.454
pubmed: 16657818
pmcid: 396886
Lamport DT, Kieliszewski MJ, Chen Y, Cannon MC (2011) Role of the Extensin superfamily in primary cell wall architecture. Plant Physiol 156(1):11–19. https://doi.org/10.1104/pp.110.169011
doi: 10.1104/pp.110.169011
pubmed: 21415277
pmcid: 3091064
Lara-Mondragón CM, Dorchak A, MacAlister CA (2022) O-glycosylation of the extracellular domain of pollen class I formins modulates their plasma membrane mobility. J Exp Bot 73(12):3929–3945. https://doi.org/10.1093/jxb/erac131
doi: 10.1093/jxb/erac131
pubmed: 35383367
pmcid: 9232206
Leroux C, Bouton S, Fabrice TN, Mareck A, Guénin S, Fournet F, Ringli C, Pelloux J, Driouich A, Lerouge P, Lehner A, Mollet J (2015) PECTIN METHYLESTERASE48 is involved in Arabidopsis pollen grain germination. Plant Physiol 167:367–380. https://doi.org/10.1104/pp.114.250928
doi: 10.1104/pp.114.250928
pubmed: 25524442
Levesque-Tremblay G, Pelloux J, Braybrook SA, Müller K (2015) Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta 242(4):791–811. https://doi.org/10.1007/s00425-015-2358-5
doi: 10.1007/s00425-015-2358-5
pubmed: 26168980
Li WL, Liu Y, Douglas CJ (2017) Role of glycosyltransferases in pollen wall primexine formation and exine patterning. Plant Physiol 173(1):167–182. https://doi.org/10.1104/pp.16.00471
doi: 10.1104/pp.16.00471
pubmed: 27495941
Lyu M, Yu Y, Jiang J, Song L, Liang Y, Ma Z, Xiong X, Cao J (2015) BcMF26a and BcMF26b are duplicated polygalacturonase genes with divergent expression patterns and functions in pollen development and pollen tube formation in Brassica campestris. PLoS ONE. https://doi.org/10.1371/journal.pone.0131173
doi: 10.1371/journal.pone.0131173
pubmed: 26713611
pmcid: 4695077
MacAlister CA, Ortiz-Ramírez C, Becker JD, Feijõ JA, Lippman ZB (2016) Hydroxyproline O-arabinosyltransferase mutants oppositely alter tip growth in Arabidopsis thaliana and Physcomitrella patens. Plant J 85(2):193–208. https://doi.org/10.1111/tpj.13079
doi: 10.1111/tpj.13079
pubmed: 26577059
Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A, Gagliardini V, Martinez-Bernardini A, Fabrice TN, Ringli C, Muschietti JP, Grossniklaus U (2017) RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358:1600–1603. https://doi.org/10.1126/science.aao5467
doi: 10.1126/science.aao5467
pubmed: 29242232
Meissner R, Jacobson Y, Melamed S, Levyatuv S, Shalev G, Ashri A, Elkind Y, Levy A (1997) A new model system for tomato genetics. Plant J 12(6):1465–1472
doi: 10.1046/j.1365-313x.1997.12061465.x
Mi L, Mo A, Yang J, Liu H, Ren D, Chen W, Long H, Jiang N, Zhang T, Lu P (2022) Arabidopsis Novel Microgametophyte Defective Mutant 1 is required for pollen viability via influencing intine development in Arabidopsis. Front Plant Sci 12(13):814870. https://doi.org/10.3389/fpls.2022.814870
doi: 10.3389/fpls.2022.814870
Møller SR, Yi X, Velásquez SM, Gille S, Hansen PLM, Poulsen CP, Olsen CE, Rejzek M, Parsons H, Yang Z, Wandall HH, Clausen H, Field RA, Pauly M, Estevez JM, Harholt J, Ulvskov P, Petersen BL (2017) Identification and evolution of a plant cell wall specific glycoprotein glycosyl transferase, ExAD. Sci Rep 7(1):45341. https://doi.org/10.1038/srep45341
doi: 10.1038/srep45341
pubmed: 28358137
pmcid: 5371791
Moon S, Kim SR, Zhao G, Yi J, Yoo Y, Jin P, Lee SW, Jung K, Zhang D, An G (2013) Rice GLYCOSYLTRANSFERASE1 encodes a glycosyltransferase essential for pollen wall formation. Plant Physiol 161(2):663–675. https://doi.org/10.1104/pp.112.210948
doi: 10.1104/pp.112.210948
pubmed: 23263792
Moore JP, Farrant JM, Driouich A (2008) A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal Behav 3(2):102–104. https://doi.org/10.4161/psb.3.2.4959
doi: 10.4161/psb.3.2.4959
pubmed: 19704722
pmcid: 2633992
Nelson BK, Cai X, Nebenfu A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136. https://doi.org/10.1111/j.1365-313X.2007.03212.x
doi: 10.1111/j.1365-313X.2007.03212.x
pubmed: 17666025
Nuñez A, Fishman ML, Fortis LL, Cooke PH, Hotchkiss AT (2009) Identification of extensin protein associated with sugar beet pectin. J Agric Food Chem 57(22):10951–10958. https://doi.org/10.1021/jf902162t
doi: 10.1021/jf902162t
pubmed: 19860469
Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y (2013) Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat Chem Biol 9(11):726–730. https://doi.org/10.1038/nchembio.1351
doi: 10.1038/nchembio.1351
pubmed: 24036508
Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5(8):578–580. https://doi.org/10.1038/nchembio.182
doi: 10.1038/nchembio.182
pubmed: 19525968
Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA 104(39):15566–15571. https://doi.org/10.1073/pnas.0706592104
doi: 10.1073/pnas.0706592104
pubmed: 17878302
pmcid: 2000526
Petersen BL, Macalister CA, Ulvskov P (2021) Plant Protein O-Arabinosylation. Front Plant Sci. https://doi.org/10.3389/fpls.2021.645219
doi: 10.3389/fpls.2021.645219
pubmed: 34790217
pmcid: 8591175
Peterson R, Slovin JP, Chen C (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol 1(2):66–69. https://doi.org/10.4081/pb.2010.e13
doi: 10.4081/pb.2010.e13
Phan HA, Iacuone S, Li SF, Parish RW (2011) The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. Plant Cell 23(6):2209–2224. https://doi.org/10.1105/tpc.110.082651
doi: 10.1105/tpc.110.082651
pubmed: 21673079
pmcid: 3160043
Piffanelli P, Ross JHE, Murphy DJ (1997) Intra- and extracellular lipid composition and associated gene expression patterns during pollen development in Brassica napus. Plant J 11(3):549–562. https://doi.org/10.1046/j.1365-313X.1997.11030549.x
doi: 10.1046/j.1365-313X.1997.11030549.x
pubmed: 9107041
Quilichini TD, Grienenberger E, Douglas CJ (2015) The biosynthesis, composition and assembly of the outer pollen wall: a tough case to crack. Phytochemistry 113:170–182. https://doi.org/10.1016/j.phytochem.2014.05.002
doi: 10.1016/j.phytochem.2014.05.002
pubmed: 24906292
Rautengarten C, Ebert B, Herter T, Petzold CJ, Ishii T, Mukhopadhyay A, Usadel B, Scheller HV (2011) The interconversion of UDP-arabinopyranose and UDP-arabinofuranose is indispensable for plant development in Arabidopsis. Plant Cell 23(4):1373–1390. https://doi.org/10.1105/tpc.111.083931
doi: 10.1105/tpc.111.083931
pubmed: 21478444
pmcid: 3101560
Renzaglia KS, Lopez RA, Welsh RD, Owen HA, Merced A (2020) Callose in sporogenesis: novel composition of the inner spore wall in hornworts. Plant Syst Evol 306(2):1–9. https://doi.org/10.1007/s00606-020-01631-5
doi: 10.1007/s00606-020-01631-5
Rubinstein AL, Marquez J, Suarez-Cervera M, Bedinger PA (1995) Extensin-like glycoproteins in the maize pollen tube wall. Plant Cell 7(12):2211–2225. https://doi.org/10.1105/tpc.7.12.2211
doi: 10.1105/tpc.7.12.2211
pubmed: 12242372
pmcid: 161074
Schnurr JA, Storey KK, Jung H-JG, Somers DA, Gronwald JW (2006) UDP-sugar pyrophosphorylase is essential for pollen development in Arabidopsis. Planta 224(3):520–532. https://doi.org/10.1007/s00425-006-0240-1
doi: 10.1007/s00425-006-0240-1
pubmed: 16557401
Sede AR, Borassi C, Wengier DL, Mecchia MA, Estevez JM, Muschietti JP (2018) Arabidopsis pollen extensins LRX are required for cell wall integrity during pollen tube growth. FEBS Lett 592(2):233–243. https://doi.org/10.1002/1873-3468.12947
doi: 10.1002/1873-3468.12947
pubmed: 29265366
Shi J, Cui M, Yang L, Kim YJ, Zhang D (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci 20(11):741–753. https://doi.org/10.1016/j.tplants.2015.07.010
doi: 10.1016/j.tplants.2015.07.010
pubmed: 26442683
Shim S-H, Mahong B, Lee S-K, Kongdin M, Lee C, Kim Y-J, Qu G, Zhang D, Cairns JRK, Jeon J-S (2022) Rice β-glucosidase Os12BGlu38 is required for synthesis of intine cell wall and pollen fertility. J Exp Bot 73(3):784–800. https://doi.org/10.1093/jxb/erab439
doi: 10.1093/jxb/erab439
pubmed: 34570888
Shimada TL, Shimada T, Hara-Nishimura I (2010) A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana: TECHNICAL ADVANCE. Plant J 61(3):519–528. https://doi.org/10.1111/j.1365-313X.2009.04060.x
doi: 10.1111/j.1365-313X.2009.04060.x
pubmed: 19891705
Shinohara H, Matsubayashi Y (2013) Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity. Plant Cell Physiol 54(3):369–374. https://doi.org/10.1093/pcp/pcs174
doi: 10.1093/pcp/pcs174
pubmed: 23256149
Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol 153(2):485–513. https://doi.org/10.1104/pp.110.156554
doi: 10.1104/pp.110.156554
pubmed: 20395450
pmcid: 2879790
Shpak E, Leykam JF, Kieliszewski MJ (1999) Synthetic genes for glycoprotein design and the elucidation of hydroxyproline-O-glycosylation codes. Proc Natl Acad Sci USA 96(26):14736–14741. https://doi.org/10.1073/pnas.96.26.14736
doi: 10.1073/pnas.96.26.14736
pubmed: 10611282
pmcid: 24717
Silva J, Ferraz R, Dupree P, Showalter AM, Coimbra S (2020) Three decades of advances in Arabinogalactan-Protein biosynthesis. Front Plant Sci 11:610377. https://doi.org/10.3389/fpls.2020.610377
doi: 10.3389/fpls.2020.610377
pubmed: 33384708
pmcid: 7769824
Stafstrom JP, Staehelin LA (1986) The role of carbohydrate in maintaining extensin in an extended conformation. Plant Physiol 81(1):242–246. https://doi.org/10.1104/pp.81.1.242
doi: 10.1104/pp.81.1.242
pubmed: 16664782
pmcid: 1075313
Suárez-Cervera M, Arcalís E, Le Thomas A, Seoane-Camba JA (2002) Pectin distribution pattern in the apertural intine of Euphorbia peplus L. (Euphorbiaceae) pollen. Sex Plant Reprod 14(5):291–298. https://doi.org/10.1007/s00497-001-0121-5
doi: 10.1007/s00497-001-0121-5
Sumiyoshi M, Inamura T, Nakamura A, Aohara T, Ishii T, Satoh S, Iwai H (2015) UDP-Arabinopyranose mutase 3 is required for pollen wall morphogenesis in rice (Oryza sativa). Plant Cell Physiol 56(2):232–241. https://doi.org/10.1093/pcp/pcu132
doi: 10.1093/pcp/pcu132
pubmed: 25261533
Takebe N, Nakamura A, Watanabe T, Miyashita A, Satoh S, Iwai H (2020) Cell wall Glycine-rich Protein2 is involved in tapetal differentiation and pollen maturation. J Plant Res 133(6):883–895. https://doi.org/10.1007/s10265-020-01223-x
doi: 10.1007/s10265-020-01223-x
pubmed: 32929552
Ueda K, Yoshimura F, Miyao A, Hirochika H, Nonomura K-I, Wabiko H (2013) Collapsed abnormal pollen1 gene encoding the Arabinokinase-like protein is involved in pollen development in rice. Plant Physiol 162(2):858–871. https://doi.org/10.1104/pp.113.216523
doi: 10.1104/pp.113.216523
pubmed: 23629836
pmcid: 3668075
Van Holst G-J, Varner JE (1984) Reinforced polyproline II conformation in a hydroxyproline-rich cell wall glycoprotein from carrot root. Plant Physiol 74:247–251
doi: 10.1104/pp.74.2.247
pubmed: 16663405
pmcid: 1066663
Van Damme D, Coutuer S, De Rycke R, Bouget F-Y, Inzé D, Geelen D (2006) Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell 18(12):3502–3518. https://doi.org/10.1105/tpc.106.040923
doi: 10.1105/tpc.106.040923
pubmed: 17189342
pmcid: 1785392
Velasquez SM, Ricardi MM, Dorosz JG, Fernandez PV, Nadra AD, Pol-Fachin L, Egelund J, Gille S, Harholt J, Ciancia M, Verli H, Pauly M, Bacic A, Olsen CE, Ulvskov P, Petersen BL, Somerville C, Iusem ND, Estevez JM (2011) O-Glycosylated cell wall proteins are essential in root hair growth. Science 332(6036):1401–1403. https://doi.org/10.1126/science.1206657
doi: 10.1126/science.1206657
pubmed: 21680836
Velasquez SM, Marzol E, Borassi C, Pol-fachin L, Ricardi MM, Mangano S, Paola S, Juarez D, Salter JDS, Dorosz JG, Marcus SE, Knox JP, Dinneny JR, Iusem ND, Verli H, Estevez JM, Fisiología ID, Molecular B (2015) Low sugar is not always good: impact of specific O-glycan defects on tip growth in Arabidopsis. Plant Physiol 168:808–813. https://doi.org/10.1104/pp.114.255521
doi: 10.1104/pp.114.255521
pubmed: 25944827
pmcid: 4741341
Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344(14):1858–1862. https://doi.org/10.1016/j.carres.2008.11.010
doi: 10.1016/j.carres.2008.11.010
pubmed: 19144326
Wang X, Wang K, Yin G, Liu X, Liu M, Cao N, Duan Y, Gao H, Wang W, Ge W, Wang J, Li R, Guo Y (2018) Pollen-expressed leucine-rich repeat extensins are essential for pollen germination and growth. Plant Physiol 176(3):1993–2006. https://doi.org/10.1104/pp.17.01241
doi: 10.1104/pp.17.01241
pubmed: 29269573
Wang J, Li M, Zhuo S, Liu Y, Yu X, Mukhtar S, Ali M, Lu G (2022) Mitogen-activated protein kinase 4 is obligatory for late pollen and early fruit development in tomato. Hortic Res. https://doi.org/10.1093/hr/uhac048
doi: 10.1093/hr/uhac048
pubmed: 37180032
pmcid: 10167419
Wolters-Arts M, Van Der Weerd L, Van Aelst AC, Van Der Weerd J, Van As H, Mariani C (2002) Water-conducting properties of lipids during pollen hydration. Plant, Cell Environ 25:513–519
doi: 10.1046/j.1365-3040.2002.00827.x
Xiong X, Zhou D, Xu L, Liu T, Yue X, Liu W, Cao J (2019) BcPME37c is involved in pollen intine formation in Brassica campestris. Biochem Biophys Res Commun 517(1):63–68
doi: 10.1016/j.bbrc.2019.07.009
pubmed: 31320138
Xu C, Liberatore KL, Macalister CA, Huang Z, Chu YH, Jiang K, Brooks C, Ogawa-Ohnishi M, Xiong G, Pauly M, Van Eck J, Matsubayashi Y, Van Der Knaap E, Lippman ZB (2015) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet 47(7):784–792. https://doi.org/10.1038/ng.3309
doi: 10.1038/ng.3309
pubmed: 26005869
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572. https://doi.org/10.1038/nprot.2007.199
doi: 10.1038/nprot.2007.199
pubmed: 17585298