We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Advertisement

Sorting nexins, a component of retromer complex, interact with SRK in Brassica oleracea

  • 30 Accesses

Abstract

Flowering plants have evolved self-incompatibility (SI) system to reject self-pollination and promote outcrossing. To further excavate SI molecular factors in Brassica oleracea, we screened pistil protein profiles. One protein spot was identified as SNX2b (sorting nexin protein 2b), which was down-regulated when expressed in cross-pollinated pistil. After cloning and sequencing SNX2b and its homologous SNX1 (sorting nexin protein 1) and SNX2a (sorting nexin protein 2a) in B. oleracea, we found that all of them contain a PX domain in N-terminal. Compared to BoSNXs (sorting nexin proteins) expression levels in reproductive organs, we found that, BoSNX1 and BoSNX2a were highly expressed in anther; however, BoSNX2b was highly expressed in pistil. qRT-PCR assays revealed that BoSNX1 and BoSNX2a showed similar expression pattern and BoSNX2b showed different expression pattern in both self- and cross-pollination process. In yeast two-hybrid assays, BoSNX1, BoSNX2a, and BoSNX2b interacted with BoSRKj (S-locus receptor kinase protein, kinase domain). Taken together, our results demonstrated that BoSNX1, BoSNX2a and BoSNX2b were differentially expressed in flower organs and in the early pollination process. On the other hand, BoSNX1, BoSNX2a, and BoSNX2b interacted with BoSRKj. Taking together, it can be suggested that BoSNX1 and BoSNX2a share similar functions but BoSNX2b plays a different role in SI response.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Barr V-A, Phillips S-A, Taylor S-I, Haft C-R (2000) Overexpression of a novel sorting nexin, SNX15, affects endosome morphology and protein trafficking. Traffic 1:904–916

  2. Carlton J, Bujny M, Rutherford A, Cullen P (2005) Sorting nexins: unifying trends and new perspectives. Traffic 6:75–82

  3. Gu T, Mazzurco M, Sulaman W, Matiad D-D, Goring D (1998) Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc Natl Acad Sci USA 95:382–387

  4. Haffani Y-Z, Gaude T, Cock J-M, Goring D-R (2004) Antisense suppression of thioredoxin h mRNA in Brassica napus cv. Westar pistils causes a low level constitutive pollen rejection response. Plant Mol Biol 55:619–630

  5. Haft C-R, Sierra M-L, Barr V-A, Haft D-H, Taylor S-I (1998) Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol Cell Biol 18:7278–7287

  6. Hanzawa T, Shibasaki K, Numata T, Kawamura Y, Gaude T, Rahman A (2013) Cellular auxin homeostasis under high temperature is regulated through a sorting nexin1-dependent endosomal trafficking pathway. Plant Cell 25(9):3424–3433

  7. Heucken and Ivanov (2018) Heucken N, Ivanov R (2018) The retromer, sorting nexins and the plant endomembrane protein trafficking. J Cell Sci. https://doi.org/10.1242/jcs.203695

  8. Indriolo E, Tharmapalan P, Wright S-I, Goring D-R (2012) The ARC1 E3 ligase gene is frequently deleted in self-compatible Brassicaceae species and has a conserved role in Arabidopsis lyrata self-pollen rejection. Plant Cell 24:4607–4620

  9. Indriolo E, Safavian D, Goring D-R (2014) The ARC1 E3 ligase promotes two different self-pollen avoidance traits in Arabidopsis. Plant Cell 26:1525–1543

  10. Ivanov R, Gaude T (2009) Endocytosis and endosomal regulation of the S-receptor kinase during the self-incompatibility response in Brassica oleracea. Plant Cell 21:2107–2117

  11. Ivanov R, Brumbarova T, Blum A, Jantke A-M, Fink-Straube C, Bauer P (2014) Sorting nexin1 is required for modulating the trafficking and stability of the Arabidopsis iron-regulated transporter1. Plant Cell 26:1294–1307

  12. Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109

  13. Jing Z, Gao Q-G, Shi S-M, Lian X-P, Converse R, Zhang H-C, Yang X-H, Ren X-S, Chen S, Zhu L-Q (2017) Dissecting pistil responses to incompatible and compatible pollen in self-incompatibility Brassica oleracea using comparative proteomics. Protein J 36:123–137

  14. Joshua C-S, Dixit M, Nasrallah M-E, Nasrallah J-B (1996) SRK, the stigma-specific S-locus receptor kinase of Brassica, is targeted to plasma membrane in transgenic tobacco. Plant Cell 8:429–445

  15. Junqiang X, Zijian S, Ming S, Qinflin T, Zhimin W, Xiaojia W (2013) Studies on the interactions between the pollen tube calmodulin (CaM) and SRK from Brassica oleracea var. capitata. Acta Hortic Sin 40(12):2429–2440

  16. Kakita M, Shimosato H, Murase K, Isogai A, Takayama S (2007) Direct interaction between S-locus receptor kinase and M-locus protein kinase involved in Brassica self-incompatibility signaling. Plant Biotechnol 24:185–190

  17. Kurten R-C, Cadena D-L, Gill G-N (1996) Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272:1008–1010

  18. Kurten R-C, Eddington A-D, Chowdhury P, Smith R-D, Davidson A-D, Shank B-B (2001) Self-assembly and binding of a sorting nexin to sorting endosomes. J Cell Sci 114(9):1743–1756

  19. Mazzurco M, Sulaman W, Elina H, Cock J-M, Goring D-R (2001) Further analysis of the interactions between the Brassica S receptor kinase and three interacting proteins (ARC1, THL1 and THL2) in the yeast. Plant Mol Biol 45:365–376

  20. Nasrallah J-B, Kao T-H, Goldberg M-L, Nasrallah M-E (1985) A cDNA clone encoding an S-locus-specific glycoprotein from Brassica oleracea. Nature 318:263–267

  21. Nasrallah J-B, Nasrallah M-E (2014) Robust self-incompatibility in the absence of a functional ARC1 gene in Arabidopsis thaliana. Plant Cell 26(10):3838–3841

  22. Parks W-T, Frank D-B, Huff C, Haft C-R, Martin J, Meng X-W, Caestecker M-P, McNally J-G, Reddi A, Taylor S-I, Roberts A-B, Wang T-W, Lechleider R-J (2001) Sorting nexin 6, a novel SNX, interacts with the transforming growth factor-β family of receptor serine-threonine kinases. J Biol Chem 276(22):19332–19339

  23. Phan N-Q, Kim S-J, Bassham D-C (2008) Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole. Mol Plant 1(6):961–976

  24. Pourcher M, Santambrogio M, Thazar N, Thierry A-M, Fobis-Loisy I, Miege C, Jaillais Y, Gaude T (2010) Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. Plant Cell 22(12):3980–3991

  25. Rojas R, Kametaka S, Haft C-R, Bonifacino J-S (2007) Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol Cell Biol 27(3):1112–1124

  26. Salanenka Y, Verstraeten I, Lofke C, Tabata K, Naramoto S, Glanc M, Friml J (2018) Gibberellin DELLA signal targets the retromer complex to redirect protein trafficking to the plasma membrane. Proc Natl Acad Sci USA 115(14):3716–3721

  27. Samuel M-A, Chong Y-T, Haasen K-E, Aldea-Brydges M-G, Stone S-L, Goring D-R (2009) Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21:2655–2671

  28. Samuel M-A, Tang W-Q, Jamshed M, Northey J, Patel D, Smith D, Siu K-W-M, Muench D-G, Wang Z- Y, Goring D-R, (2011) Proteomic analysis of Brassica stigmatic proteins following the self-incompatibility reaction reveals a role for microtubule dynamics during pollen responses. Mol Cell Proteom 10:1–13

  29. Seaman (2012) The retromer complex-endosomal protein recycling and beyond. J Cell Sci 125:4693–4702

  30. Sheoran I-S, Sproule K-A, Olson D-J-H, Ross A-R-S, Sawhney V (2006) Proteome profile and functional classification of proteins in Arabidopsis thaliana (Landsberg erecta) mature pollen. Sex Plant Reprod 19:185–196

  31. Shiba H, Takayama S, Iwano M, Shimosato H, Funato M, Nakagawa T, Suzuki G, Watanabe M, Hinata K, Isogai A (2001) A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol 125:2095–2103

  32. Stein J-C, Nasrallah J-B (1993) A plant receptor-like gene, the S-locus receptor kinase of Brassica oleracea L., encodes a functional serine/threonine kinase. Plant Physiol 101:1103–1106

  33. Stephenson A-G, Doughty J, Dixon S, Elleman C, Hiscock S, Dickinson H-G (1997) The male determinant of self-incompatibility in Brassica oleracea is located in the pollen coating. Plant J 12:1351–1359

  34. Stone S-L, Arnoldo M, Goring D-R (1999) A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286:1729–1731

  35. Stone S-L, Anderson E-M, Mullen R-T, Goring D-R (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885–898

  36. Takayama S, Shimosato H, Shiba H, Funato F-S, Chen M, Watanabe M (2001) Direct ligand receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–538

  37. Teasdale R-D, Loci D, Houghton F, Karlsson L, Gleeson P-A (2001) A large family of endosome-localized proteins related to sorting nexin 1. Biochem J 358:7–16

  38. Vanoosthuyse V, Tichtinsky G, Dumas C, Gaude T, Cock J-M (2003) Interaction of calmodulin, a sorting nexin and kinase-associated protein phosphatase with the Brassica oleracea S-locus receptor kinase. Plant Physiol 133:919–929

  39. Wang L, Peng H, Ge T, Liu T, Hou X, Li Y (2014) Identification of differentially accumulating pistil proteins associated with self-incompatibility of non-heading Chinese cabbage. Plant Biol 16:49–57

  40. Worby C-A, Dixon J-E (2002) Sorting out the cellular functions of sorting nexins. Nat Rev Mol Cell Biol 3:919–931

  41. Xu Y, Hortsman H, Seet L, Won S-H, Hong W (2001) SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns (3) P. Nat Cell Biol 3:658–666

  42. Yunlong B, Qiguo G, Songmei S, Xiaohuan L, Quanming P, Ying Z, Lincheng Z, Xiaoping L, Jing L, Liquan Z (2015) Molecular cloning of BoSU03 and analysis of the interaction between SRK and BoSU03 in Brassica oleracea. Acta Hortic Sin 42(11):2206–2214

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC 31572127), the Chongqing Natural Science Foundation (cstc2018jscx-mszd0021), the Science and Technology Research Program of Chongqing Municipal Commission (KJQN 201801433).

Author information

Correspondence to Yihua Liu or Liquan Zhu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by E. Schleiff.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zeng, J., Lian, X., Mo, Y. et al. Sorting nexins, a component of retromer complex, interact with SRK in Brassica oleracea. Acta Physiol Plant 42, 11 (2020). https://doi.org/10.1007/s11738-019-2994-7

Download citation

Keywords

  • Self- and cross-pollination
  • B. oleracea
  • Protein profiles
  • BoSNXs
  • BoSRKj
  • Interaction