Skip to main content
Log in

Purine permease (PUP) family gene PUP11 positively regulates the rice seed setting rate by influencing seed development

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Purine permease PUP11 is essential for rice seed development, regulates the seed setting rate, and influences the cytokinin content, sugar transport, and starch biosynthesis during grain development.

Abstract

The distribution of cytokinins in plant tissues determines plant growth and development and is regulated by several cytokinin transporters, including purine permease (PUP). Thirteen PUP genes have been identified within the rice genome; however, the functions of most of these genes remain poorly understood. We found that pup11 mutants showed extremely low seed setting rates and a unique filled seed distribution. Moreover, seed formation arrest in these mutants was associated with the disappearance of accumulated starch 10 days after flowering. PUP11 has two major transcripts with different expression patterns and subcellular locations, and further studies revealed that they have redundant positive roles in regulating the seed setting rate. We also found that type-A Response Regulator (RR) genes were upregulated in the developing grains of the pup11 mutant compared with those in the wild type. The results also showed that PUP11 altered the expression of several sucrose transporters and significantly upregulated certain starch biosynthesis genes. In summary, our results indicate that PUP11 influences the rice seed setting rate by regulating sucrose transport and starch accumulation during grain filling. This research provides new insights into the relationship between cytokinins and seed development, which may help improve cereal yield.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

All data supporting the findings of this study are available within the paper and within its supplementary data published online.

References

  • Basunia MA, Nonhebel HM (2019) Hormonal regulation of cereal endosperm development with a focus on rice (Oryza sativa). Funct Plant Biol 46:493–506

    Article  CAS  PubMed  Google Scholar 

  • Chang Z, Xu R, Xun Q, Liu J, Zhong T, Ding Y, Ding C (2021) OsmiR164-targeted OsNAM, a boundary gene, plays important roles in rice leaf and panicle development. Plant J Cell Mol Biol 106:41–55

    Article  CAS  Google Scholar 

  • Chen Y, Teng Z, Yuan Y, Yi Z, Zheng Q, Yu H, Lv J, Wang Y, Duan M, Zhang J, Ye N (2022) Excessive nitrogen in field-grown rice suppresses grain filling of inferior spikelets by reducing the accumulation of cytokinin and auxin. Field Crops Res 283:108542

    Article  Google Scholar 

  • Deng Y, Yu Y, Hu Y, Ma L, Lin Y, Wu Y, Wang Z, Wang Z, Bai J, Ding Y, Chen L (2021) Auxin-mediated regulation of dorsal vascular cell development may be responsible for sucrose phloem unloading in large panicle rice. Front Plant Sci 12:630997

    Article  PubMed  PubMed Central  Google Scholar 

  • Duran-Medina Y, Diaz-Ramirez D, Marsch-Martinez N (2017) Cytokinins on the Move. Front Plant Sci 8:146

    Article  PubMed  PubMed Central  Google Scholar 

  • Fei H, Yang Z, Lu Q, Wen X, Zhang Y, Zhang A, Lu C (2021) OsSWEET14 cooperates with OsSWEET11 to contribute to grain filling in rice. Plant Sci 306:110851

    Article  CAS  PubMed  Google Scholar 

  • Hirose N, Makita N, Yamaya T, Sakakibara H (2005) Functional characterization and expression analysis of a gene, OsENT2, encoding an equilibrative nucleoside transporter in rice suggest a function in cytokinin transport. Plant Physiol 138:196–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Liu J, Lin Y, Xu X, Xia Y, Bai J, Yu Y, Xiao F, Ding Y, Ding C, Chen L (2022) Sucrose nonfermenting-1-related protein kinase 1 regulates sheath-to-panicle transport of nonstructural carbohydrates during rice grain filling. Plant Physiol 189:1694–1714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Patra P, Pisanty O, Shafir A, Belew ZM, Binenbaum J, Ben Yaakov S, Shi B, Charrier L, Hyams G, Zhang Y, Trabulsky M, Caldararu O, Weiss D, Crocoll C, Avni A, Vernoux T, Geisler M, Nour-Eldin HH, Mayrose I, Shani E (2023) Multi-Knock-a multi-targeted genome-scale CRISPR toolbox to overcome functional redundancy in plants. Nature Plants 9:572–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang P, Zhao J, Hong J, Zhu B, Xia S, Zhu E, Han P, Zhang K (2023) Cytokinins regulate rice lamina joint development and leaf angle. Plant Physiol 191:56–69

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Shi X, Chang Z, Ding Y, Ding C (2022a) Auxin efflux transporters OsPIN1c and OsPIN1d function redundantly in regulating rice (Oryza sativa L.) panicle development. Plant Cell Physiol 63:305–316

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Wu MW, Liu CM (2022b) Cereal endosperms: development and storage product accumulation. Annu Rev Plant Biol 73:255–291

    Article  CAS  PubMed  Google Scholar 

  • Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu JK (2013) Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant 6:2008–2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panda BB, Sekhar S, Dash SK, Behera L, Shaw BP (2018) Biochemical and molecular characterisation of exogenous cytokinin application on grain filling in rice. BMC Plant Biol 18:89

    Article  PubMed  PubMed Central  Google Scholar 

  • Qi Z, Xiong L (2013) Characterization of a purine permease family gene OsPUP7 involved in growth and development control in rice. J Integr Plant Biol 55:1119–1135

    Article  CAS  PubMed  Google Scholar 

  • Radchuk V, Belew ZM, Gundel A, Mayer S, Hilo A, Hensel G, Sharma R, Neumann K, Ortleb S, Wagner S, Muszynska A, Crocoll C, Xu D, Hoffie I, Kumlehn J, Fuchs J, Peleke FF, Szymanski JJ, Rolletschek H, Nour-Eldin HH, Borisjuk L (2023) SWEET11b transports both sugar and cytokinin in developing barley grains. Plant Cell 35:2186–2207

    Article  PubMed  PubMed Central  Google Scholar 

  • Rong C, Liu Y, Chang Z, Liu Z, Ding Y, Ding C (2022) Cytokinin oxidase/dehydrogenase family genes exhibit functional divergence and overlap in rice growth and development, especially in control of tillering. J Exp Bot 73:3552–3568

    Article  CAS  PubMed  Google Scholar 

  • Sakakibara H (2021) Cytokinin biosynthesis and transport for systemic nitrogen signaling. Plant J 105:421–430

    Article  CAS  PubMed  Google Scholar 

  • Scofield GN, Hirose T, Gaudron JA, Furbank RT, Upadhyaya NM, Ohsugi R (2002) Antisense suppression of the rice transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis. Funct Plant Biol 29:815–826

    Article  CAS  PubMed  Google Scholar 

  • Tessi TM, Brumm S, Winklbauer E, Schumacher B, Pettinari G, Lescano I, Gonzalez CA, Wanke D, Maurino VG, Harter K, Desimone M (2021) Arabidopsis AZG2 transports cytokinins in vivo and regulates lateral root emergence. New Phytol 229:979–993

    Article  CAS  PubMed  Google Scholar 

  • Tsago Y, Chen ZY, Cao H, Sunusi M, Khan AU, Shi CH, Jin XL (2020) Rice gene, OsCKX2-2, regulates inflorescence and grain size by increasing endogenous cytokinin content. Plant Growth Regul 92:283–294

    Article  CAS  Google Scholar 

  • Tsai YC, Weir NR, Hill K, Zhang W, Kim HJ, Shiu SH, Schaller GE, Kieber JJ (2012) Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol 158:1666–1684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang E, Wang J, Zhu X, Hao W, Wang L, Li Q, Zhang L, He W, Lu B, Lin H, Ma H, Zhang G, He Z (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370–1374

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Lu Y, Guo Z, Ding Y, Ding C (2020) RICE CENTRORADIALIS 1, a TFL1-like Gene, responses to drought stress and regulates rice flowering transition. Rice (n Y) 13:70

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Wu Y, Ma L, Lin Y, Hu Y, Li M, Li W, Ding Y, Chen L (2021) Phloem loading in rice leaves depends strongly on the apoplastic pathway. J Exp Bot 72:3723–3738

    Article  CAS  PubMed  Google Scholar 

  • Wu C, Cui K, Wang W, Li Q, Fahad S, Hu Q, Huang J, Nie L, Mohapatra PK, Peng S (2017) Heat-induced cytokinin transportation and degradation are associated with reduced panicle cytokinin expression and fewer spikelets per panicle in rice. Front Plant Sci 8:371

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao Y, Liu D, Zhang G, Gao S, Liu L, Xu F, Che R, Wang Y, Tong H, Chu C (2019) Big Grain3, encoding a purine permease, regulates grain size via modulating cytokinin transport in rice. J Integr Plant Biol 61:581–597

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Zhang J, Yu G, Lu X, Mei W, Deng H, Zhang G, Chen G, Chu C, Tong H, Tang W (2020) Endoplasmic Reticulum-Localized PURINE PERMEASE1 regulates plant height and grain weight by modulating cytokinin distribution in rice. Front Plant Sci 11:618560

    Article  PubMed  PubMed Central  Google Scholar 

  • Xun Q, Mei M, Song Y, Rong C, Liu J, Zhong T, Ding Y, Ding C (2022) SWI2/SNF2 chromatin remodeling ATPases SPLAYED and BRAHMA control embryo development in rice. Plant Cell Rep 41:1389–1401

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Luo D, Yang B, Frommer WB, Eom JS (2018) SWEET11 and 15 as key players in seed filling in rice. New Phytol 218:604–615

    Article  CAS  PubMed  Google Scholar 

  • You C, Zhu H, Xu B, Huang W, Wang S, Ding Y, Liu Z, Li G, Chen L, Ding C, Tang S (2016) Effect of removing superior spikelets on grain filling of inferior spikelets in rice. Front Plant Sci 7:1161

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang K, Novak O, Wei Z, Gou M, Zhang X, Yu Y, Yang H, Cai Y, Strnad M, Liu CJ (2014) Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat Commun 5:3274

    Article  PubMed  Google Scholar 

  • Zhang W, Peng K, Cui F, Wang D, Zhao J, Zhang Y, Yu N, Wang Y, Zeng D, Wang Y, Cheng Z, Zhang K (2021) Cytokinin oxidase/dehydrogenase OsCKX11 coordinates source and sink relationship in rice by simultaneous regulation of leaf senescence and grain number. Plant Biotechnol J 19:335–350

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Berman A, Shani E (2023) Plant hormone transport and localization: signaling molecules on the move. Annu Rev Plant Biol 74:453–479

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Yu N, Ju M, Fan B, Zhang Y, Zhu E, Zhang M, Zhang K (2019) ABC transporter OsABCG18 controls the shootward transport of cytokinins and grain yield in rice. J Exp Bot 70:6277–6291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zurcher E, Muller B (2016) Cytokinin synthesis, signaling, and function-advances and new insights. Int Rev Cell Mol Biol 324:1–38

    Article  CAS  PubMed  Google Scholar 

  • Zurcher E, Liu J, di Donato M, Geisler M, Muller B (2016) Plant development regulated by cytokinin sinks. Science 353:1027–1030

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Jiankang Zhu and Caixia Gao for providing the vectors of the CRISPR-Cas9 system. We also thank Biogle and Biorun genome editing center for producing transgenic rice.

Funding

This work was supported by the Natural Science Foundation of Jiangsu Province (Grants no BK20231470).

Author information

Authors and Affiliations

Authors

Contributions

C.D. and Y.D. conceived the original screening and research plans; C.R., R.Z., Y.L., Z.C., Z.L., and C.D. performed the experiments and analyzed the data; C.R. and C.D. wrote the article with contributions of all the authors; C.D. agrees to serve as the author responsible for contact and ensures communication.

Corresponding authors

Correspondence to Yanfeng Ding or Chengqiang Ding.

Ethics declarations

Conflict of interest

The authors declare no competing interests in relation to this work.

Additional information

Communicated by Andrew Leigh Eamens.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 6613 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rong, C., Zhang, R., Liu, Y. et al. Purine permease (PUP) family gene PUP11 positively regulates the rice seed setting rate by influencing seed development. Plant Cell Rep 43, 112 (2024). https://doi.org/10.1007/s00299-024-03193-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00299-024-03193-z

Keywords

Navigation