The canonical α-SNAP is essential for gametophytic development in Arabidopsis

English version

Autoři: Fei Liu ^aff001; Ji-Peng Li ^aff002; Lu-Shen Li ^aff002; Qi Liu ^aff002; Shan-Wei Li ^aff002; Ming-Lei Song ^aff002; Sha Li ^aff001; Yan Zhang ^aff002
Působiště autorů: Department of Plant Biology and Ecology, College of Life Sciences, Nankai University, Tianjin, China ^aff001; State Key laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an, China ^aff002
Vyšlo v časopise: The canonical α-SNAP is essential for gametophytic development in Arabidopsis. PLoS Genet 17(4): e1009505. doi:10.1371/journal.pgen.1009505
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009505

Souhrn

The development of male and female gametophytes is a pre-requisite for successful reproduction of angiosperms. Factors mediating vesicular trafficking are among the key regulators controlling gametophytic development. Fusion between vesicles and target membranes requires the assembly of a fusogenic soluble N-ethylmaleimide sensitive factor attachment protein receptors (SNAREs) complex, whose disassembly in turn ensures the recycle of individual SNARE components. The disassembly of post-fusion SNARE complexes is controlled by the AAA⁺ ATPase N-ethylmaleimide-sensitive factor (Sec18/NSF) and soluble NSF attachment protein (Sec17/α-SNAP) in yeast and metazoans. Although non-canonical α-SNAPs have been functionally characterized in soybeans, the biological function of canonical α-SNAPs has yet to be demonstrated in plants. We report here that the canonical α-SNAP in Arabidopsis is essential for male and female gametophytic development. Functional loss of the canonical α-SNAP in Arabidopsis results in gametophytic lethality by arresting the first mitosis during gametogenesis. We further show that Arabidopsis α-SNAP encodes two isoforms due to alternative splicing. Both isoforms interact with the Arabidopsis homolog of NSF whereas have distinct subcellular localizations. The presence of similar alternative splicing of human α-SNAP indicates that functional distinction of two α-SNAP isoforms is evolutionarily conserved.

Klíčová slova:

Anthers – Arabidopsis thaliana – Confocal laser microscopy – DAPI staining – Ovules – Plant genomics – Pollen – Embryo sac

Zdroje

1. Drews GN, Yadegari R (2002) Development and function of the angiosperm female gametophyte. Annu Rev Genet 36: 99–124. doi: 10.1146/annurev.genet.36.040102.131941 12429688

2. McCormick S (1993) Male gametophyte development. Plant Cell 5: 1265–1275. doi: 10.1105/tpc.5.10.1265 12271026

3. McCormick S (2004) Control of male gametophyte development. Plant Cell 16 Suppl: S142–153. doi: 10.1105/tpc.016659 15037731

4. Liu J, Zhang Y, Qin G, Tsuge T, Sakaguchi N, et al. (2008) Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. Plant Cell 20: 1538–1554. doi: 10.1105/tpc.108.059741 18552199

5. Liu J, Qu LJ (2008) Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol Plant 1: 564–574. doi: 10.1093/mp/ssn033 19825562

6. Nowack MK, Harashima H, Dissmeyer N, Zhao X, Bouyer D, et al. (2012) Genetic framework of cyclin-dependent kinase function in Arabidopsis. Dev Cell 22: 1030–1040. doi: 10.1016/j.devcel.2012.02.015 22595674

7. Takatsuka H, Umeda-Hara C, Umeda M (2015) Cyclin-dependent kinase-activating kinases CDKD;1 and CDKD;3 are essential for preserving mitotic activity in Arabidopsis thaliana. Plant J 82: 1004–1017. doi: 10.1111/tpj.12872 25942995

8. Xiong F, Duan CY, Liu HH, Wu JH, Zhang ZH, et al. (2020) Arabidopsis KETCH1 is critical for the nuclear accumulation of ribosomal proteins and gametogenesis. Plant Cell 32: 1270–1284. doi: 10.1105/tpc.19.00791 32086364

9. Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, et al. (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17: 2340–2354. doi: 10.1105/tpc.105.033563 15980260

10. Li N, Yuan L, Liu N, Shi D, Li X, et al. (2009) SLOW WALKER2, a NOC1/MAK21 homologue, is essential for coordinated cell cycle progression during female gametophyte development in Arabidopsis. Plant Physiol 151: 1486–1497. doi: 10.1104/pp.109.142414 19734265

11. Falcone Ferreyra ML, Casadevall R, Luciani MD, Pezza A, Casati P (2013) New evidence for differential roles of l10 ribosomal proteins from Arabidopsis. Plant Physiol 163: 378–391. doi: 10.1104/pp.113.223222 23886624

12. Falcone Ferreyra ML, Pezza A, Biarc J, Burlingame AL, Casati P (2010) Plant L10 ribosomal proteins have different roles during development and translation under ultraviolet-B stress. Plant Physiol 153: 1878–1894. doi: 10.1104/pp.110.157057 20516338

13. Feng C, Wang JG, Liu HH, Li S, Zhang Y (2017) Arabidopsis adaptor protein 1G is critical for pollen development. J Integr Plant Biol 59: 594–599. doi: 10.1111/jipb.12556 28544342

14. Zhang WT, Li E, Guo YK, Yu SX, Wan ZY, et al. (2018) Arabidopsis VAC14 is critical for pollen development through mediating vacuolar organization. Plant Physiol 177: 1529–1538. doi: 10.1104/pp.18.00495 29884680

15. Whitley P, Hinz S, Doughty J (2009) Arabidopsis FAB1/PIKfyve proteins are essential for development of viable pollen. Plant Physiol 151: 1812–1822. doi: 10.1104/pp.109.146159 19846542

16. Dettmer J, Schubert D, Calvo-Weimar O, Stierhof YD, Schmidt R, et al. (2005) Essential role of the V-ATPase in male gametophyte development. Plant J 41: 117–124. doi: 10.1111/j.1365-313X.2004.02282.x 15610354

17. Bolanos-Villegas P, Guo CL, Jauh GY (2015) Arabidopsis Qc-SNARE genes BET11 and BET12 are required for fertility and pollen tube elongation. Bot Stud 56: 21. doi: 10.1186/s40529-015-0102-x 28510830

18. El-Kasmi F, Pacher T, Strompen G, Stierhof YD, Muller LM, et al. (2011) Arabidopsis SNARE protein SEC22 is essential for gametophyte development and maintenance of Golgi-stack integrity. Plant J 66: 268–279. doi: 10.1111/j.1365-313X.2011.04487.x 21205036

19. Uemura T, Morita MT, Ebine K, Okatani Y, Yano D, et al. (2010) Vacuolar/pre-vacuolar compartment Qa-SNAREs VAM3/SYP22 and PEP12/SYP21 have interchangeable functions in Arabidopsis. Plant J 64: 864–873. doi: 10.1111/j.1365-313X.2010.04372.x 21105932

20. Bassham DC, Brandizzi F, Otegui MS, Sanderfoot AA (2008) The secretory system of Arabidopsis. Arabidopsis Book 6: e0116. doi: 10.1199/tab.0116 22303241

21. Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144: 6–17. doi: 10.1104/pp.106.092973 17369437

22. Zhang L, Li W, Wang T, Zheng F, Li J (2015) Requirement of R-SNAREs VAMP721 and VAMP722 for the gametophyte activity, embryogenesis and seedling root development in Arabidopsis. Plant Growth Regul 77: 57–65.

23. Ma T, Li E, Li LS, Li S, Zhang Y (2020) The Arabidopsis R-SNARE protein YKT61 is essential for gametophyte development. J Integr Plant Biol doi: 10.1111/jipb.13017 32918784

24. Bombardier JP, Munson M (2015) Three steps forward, two steps back: mechanistic insights into the assembly and disassembly of the SNARE complex. Curr Opin Chem Biol 29: 66–71. doi: 10.1016/j.cbpa.2015.10.003 26498108

25. Ryu JK, Jahn R, Yoon TY (2016) Review: Progresses in understanding N-ethylmaleimide sensitive factor (NSF) mediated disassembly of SNARE complexes. Biopolymers 105: 518–531. doi: 10.1002/bip.22854 27062050

26. Winter U, Chen X, Fasshauer D (2009) A conserved membrane attachment site in alpha-SNAP facilitates N-ethylmaleimide-sensitive factor (NSF)-driven SNARE complex disassembly. J Biol Chem 284: 31817–31826. doi: 10.1074/jbc.M109.045286 19762473

27. Miao Y, Miner C, Zhang L, Hanson PI, Dani A, et al. (2013) An essential and NSF independent role for alpha-SNAP in store-operated calcium entry. Elife 2: e00802. doi: 10.7554/eLife.00802 23878724

28. Wang L, Brautigan DL (2013) α-SNAP inhibits AMPK signaling to reduce mitochondrial biogenesis and dephosphorylates Thr172 in AMPKα in vitro. Nat Commun 4: 1559. doi: 10.1038/ncomms2565 23463002

29. Bayless AM, Smith JM, Song J, McMinn PH, Teillet A, et al. (2016) Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean <em>Rhg1</em&gt. Proceedings of the National Academy of Sciences 113: E7375. doi: 10.1073/pnas.1610150113 27821740

30. Bayless AM, Zapotocny RW, Grunwald DJ, Amundson KK, Diers BW, et al. (2018) An atypical N-ethylmaleimide sensitive factor enables the viability of nematode-resistant Rhg1 soybeans. Proc Natl Acad Sci U S A 115: E4512–E4521. doi: 10.1073/pnas.1717070115 29695628

31. Matsye PD, Lawrence GW, Youssef RM, Kim KH, Lawrence KS, et al. (2012) The expression of a naturally occurring, truncated allele of an α-SNAP gene suppresses plant parasitic nematode infection. Plant Mol Biol 80: 131–155. doi: 10.1007/s11103-012-9932-z 22689004

32. Lakhssassi N, Liu S, Bekal S, Zhou Z, Colantonio V, et al. (2017) Characterization of the Soluble NSF Attachment Protein gene family identifies two members involved in additive resistance to a plant pathogen. Sci Rep 7: 45226. doi: 10.1038/srep45226 28338077

33. Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167–170. doi: 10.1126/science.1179555 20056882

34. Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157: 1262–1278. doi: 10.1016/j.cell.2014.05.010 24906146

35. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, et al. (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14: 327. doi: 10.1186/s12870-014-0327-y 25432517

36. Yang X, Zhang Q, Zhao K, Luo Q, Bao S, et al. (2017) The Arabidopsis GPR1 Gene Negatively Affects Pollen Germination, Pollen Tube Growth, and Gametophyte Senescence. International journal of molecular sciences 18: 1303.

37. Marz KE, Lauer JM, Hanson PI (2003) Defining the SNARE complex binding surface of alpha-SNAP: implications for SNARE complex disassembly. J Biol Chem 278: 27000–27008. doi: 10.1074/jbc.M302003200 12730228

38. Lam SK, Cai Y, Tse YC, Wang J, Law AH, et al. (2009) BFA-induced compartments from the Golgi apparatus and trans-Golgi network/early endosome are distinct in plant cells. Plant J 60: 865–881. doi: 10.1111/j.1365-313X.2009.04007.x 19709389

39. Wang JG, Feng C, Liu HH, Ge FR, Li S, et al. (2016) HAPLESS13-mediated trafficking of STRUBBELIG is critical for ovule development in Arabidopsis. PLoS Genet 12: e1006269. doi: 10.1371/journal.pgen.1006269 27541731

40. Lee GJ, Sohn EJ, Lee MH, Hwang I (2004) The Arabidopsis Rab5 homologs Rha1 and Ara7 localize to the prevacuolar compartment. Plant Cell Physiol 45: 1211–1220. doi: 10.1093/pcp/pch142 15509844

41. Geldner N, Denervaud-Tendon V, Hyman DL, Mayer U, Stierhof YD, et al. (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 59: 169–178. doi: 10.1111/j.1365-313X.2009.03851.x 19309456

42. Ryu JK, Min D, Rah SH, Kim SJ, Park Y, et al. (2015) Spring-loaded unraveling of a single SNARE complex by NSF in one round of ATP turnover. Science 347: 1485–1489. doi: 10.1126/science.aaa5267 25814585

43. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621–2632. doi: 10.1104/pp.104.046367 15375207

44. Choi UB, Zhao M, White KI, Pfuetzner RA, Esquivies L, et al. (2018) NSF-mediated disassembly of on- and off-pathway SNARE complexes and inhibition by complexin. Elife 7.

45. Yu RC, Jahn R, Brunger AT (1999) NSF N-Terminal Domain Crystal Structure: Models of NSF Function. Molecular Cell 4: 97–107. doi: 10.1016/s1097-2765(00)80191-4 10445031

46. Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T (2003) Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol 44: 1192–1201. doi: 10.1093/pcp/pcg147 14634156

47. Christensen CA, King EJ, Jordan JR, Drews GN (1997) Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex Plant Reprod 10: 49–64.

48. Drews GN, Lee D, Christensen CA (1998) Genetic analysis of female gametophyte development and function. Plant Cell 10: 5–17. doi: 10.1105/tpc.10.1.5 9477569

49. D’Ippolito S, Arias LA, Casalongue CA, Pagnussat GC, Fiol DF (2017) The DC1-domain protein VACUOLELESS GAMETOPHYTES is essential for development of female and male gametophytes in Arabidopsis. Plant J 90: 261–275. doi: 10.1111/tpj.13486 28107777

50. Tanaka Y, Nishimura K, Kawamukai M, Oshima A, Nakagawa T (2013) Redundant function of two Arabidopsis COPII components, AtSec24B and AtSec24C, is essential for male and female gametogenesis. Planta 238: 561–575. doi: 10.1007/s00425-013-1913-1 23779001

51. Liang X, Li SW, Gong LM, Li S, Zhang Y (2020) COPII components Sar1b and Sar1c play distinct yet interchangeable roles in pollen development. Plant Physiol 183: 974–985. doi: 10.1104/pp.20.00159 32327549

52. Zhou LZ, Li S, Feng QN, Zhang YL, Zhao X, et al. (2013) PROTEIN S-ACYL TRANSFERASE10 is critical for development and salt tolerance in Arabidopsis. Plant Cell 25: 1093–1107. doi: 10.1105/tpc.112.108829 23482856

53. Li S, Ge F-R, Xu M, Zhao X-Y, Huang G-Q, et al. (2013) Arabidopsis COBRA-LIKE 10, a GPI-anchored protein, mediates directional growth of pollen tubes. The Plant Journal 74: 486–497. doi: 10.1111/tpj.12139 23384085

54. Pagnussat GC, Yu H-J, Ngo QA, Rajani S, Mayalagu S, et al. (2005) Genetic and molecular identification of genes required for female gametophyte development and function in <em>Arabidopsis</em&gt. Development 132: 603. doi: 10.1242/dev.01595 15634699

55. Wang J-G, Feng C, Liu H-H, Feng Q-N, Li S, et al. (2017) AP1G mediates vacuolar acidification during synergid-controlled pollen tube reception. Proceedings of the National Academy of Sciences 114: E4877. doi: 10.1073/pnas.1617967114 28559348

56. Huang G-Q, Li E, Ge F-R, Li S, Wang Q, et al. (2013) Arabidopsis RopGEF4 and RopGEF10 are important for FERONIA-mediated developmental but not environmental regulation of root hair growth. New Phytologist 200: 1089–1101.

57. Martin K, Kopperud K, Chakrabarty R, Banerjee R, Brooks R, et al. (2009) Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. The Plant Journal 59: 150–162. doi: 10.1111/j.1365-313X.2009.03850.x 19309457

58. Li E, Cui Y, Ge F-R, Chai S, Zhang W-T, et al. (2018) AGC1.5 Kinase Phosphorylates RopGEFs to Control Pollen Tube Growth. Molecular Plant 11: 1198–1209. doi: 10.1016/j.molp.2018.07.004 30055264

59. Liu H-H, Xiong F, Duan C-Y, Wu Y-N, Zhang Y, et al. (2019) Importin β4 Mediates Nuclear Import of GRF-Interacting Factors to Control Ovule Development in Arabidopsis. Plant Physiology 179: 1080. doi: 10.1104/pp.18.01135 30659067

60. Ma T, Li E, Li L-S, Li S, Zhang Y (2020) The Arabidopsis R-SNARE protein YKT61 is essential for gametophyte development. Journal of Integrative Plant Biology n/a. doi: 10.1111/jipb.13017 32918784

61. Zhang YL, Li E, Feng QN, Zhao XY, Ge FR, et al. (2015) Protein palmitoylation is critical for the polar growth of root hairs in Arabidopsis. BMC Plant Biol 15: 50. doi: 10.1186/s12870-015-0441-5 25849075

62. Li E, Zhang YL, Shi X, Li H, Yuan X, et al. (2020) A positive feedback circuit for ROP-mediated polar growth. Mol Plant doi: 10.1016/j.molp.2020.11.017 33271334

63. Feng Q-N, Kang H, Song S-J, Ge F-R, Zhang Y-L, et al. (2016) Arabidopsis RhoGDIs Are Critical for Cellular Homeostasis of Pollen Tubes. Plant Physiology 170: 841. doi: 10.1104/pp.15.01600 26662604

64. Xie H-T, Wan Z-Y, Li S, Zhang Y (2014) Spatiotemporal Production of Reactive Oxygen Species by NADPH Oxidase Is Critical for Tapetal Programmed Cell Death and Pollen Development in <em>Arabidopsis</em&gt. The Plant Cell 26: 2007. doi: 10.1105/tpc.114.125427 24808050

65. Feng Q-N, Liang X, Li S, Zhang Y (2018) The ADAPTOR PROTEIN-3 Complex Mediates Pollen Tube Growth by Coordinating Vacuolar Targeting and Organization. Plant Physiology 177: 216. doi: 10.1104/pp.17.01722 29523712

66. Wan ZY, Chai S, Ge FR, Feng QN, Zhang Y, et al. (2017) Arabidopsis PROTEIN S-ACYL TRANSFERASE4 mediates root hair growth. Plant J 90: 249–260. doi: 10.1111/tpj.13484 28107768

67. Chai S, Ge F-R, Feng Q-N, Li S, Zhang Y (2016) PLURIPETALA mediates ROP2 localization and stability in parallel to SCN1 but synergistically with TIP1 in root hairs. The Plant Journal 86: 413–425. doi: 10.1111/tpj.13179 27037800

Článek Analysis of cell-type-specific chromatin modifications and gene expression in Drosophila neurons that direct reproductive behavior

Článek Virus-derived variation in diverse human genomes

Článek Aurora kinase A is essential for meiosis in mouse oocytes

Článek Pathways and signatures of mutagenesis at targeted DNA nicks

Článek A complex genetic architecture in zebrafish relatives Danio quagga and D. kyathit underlies development of stripes and spots

Článek Genetic analysis of the septal peptidoglycan synthase FtsWI complex supports a conserved activation mechanism for SEDS-bPBP complexes

Článek Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers

Článek Toxic Y chromosome: Increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome

Článek MRLocus: Identifying causal genes mediating a trait through Bayesian estimation of allelic heterogeneity

Článek Tissue specificity-aware TWAS (TSA-TWAS) framework identifies novel associations with metabolic, immunologic, and virologic traits in HIV-positive adults

Článek Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination

Článek Control of pre-replicative complex during the division cycle in Chlamydomonas reinhardtii