Skip to main content
Log in

The phosphoinositide-specific phospholipase C1 modulates flowering time and grain size in rice

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Preferential expression of OsPLC1 is detected at the heading stage of rice, OsPLC1 overexpression results in early flowering, increased-grain size and yield; however, opposing phenotypes produced in the osplc1 mutants.

Abstract: The importance of phospholipase C (PLC) in plant development has been demonstrated in several studies. OsPLC1, a member of PI-PLC in rice, although its role in the response to salt stress of rice seedlings has been reported, its functions in the growth and development of rice is elusive. Here, we report that OsPLC1 expression could be detectable in various tissues throughout the developmental stages of rice, and the highest expression level of OsPLC1 was detected at the heading stage. OsPLC1 overexpression (OE) produced rice plants with early flowering, whereas OsPLC1 loss-of-function led to delay in flowering. The expression levels of subset genes, which are involved in the control of flowering time in rice, were altered in the plants of OE and osplc1. In addition, the enlargement of grain size was observed in OE plants, however, the reduction of grain size was noticed in osplc1 mutants. The increase in the grain size and the grain yield of OE lines were associated with the improvement of cell length and expression levels of a set of genes related to cell expansion, contrarily, the decrease in osplc1 mutant grain size and yield were linked to declined cell length and expression levels of related genes. No significant differences, in terms of the grain quality of mature seeds, were found in OE and osplc1 mutants, with compared to those in Nipponbare (Nip). In summary, our study suggests that OsPLC1 could modulate rice flowering time and grain size.

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

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Aya K, Hobo T, Sato-Izawa K, Ueguchi-Tanaka M, Kitano H, Matsuoka M (2014) A novel AP2-type transcription factor, SMALL ORGAN SIZE1, controls organ size downstream of an auxin signaling pathway. Plant Cell Physiol 55:897–912

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Łyskowski A, Jaremko Ł, Jaremko M (2021) Genetic and molecular factors determining grain weight in rice. Front Plant Sci 12:605799

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen X, Li L, Xu B, Zhao S, Lu P, He Y, Ye T, Feng YQ, Wu Y (2019) Phosphatidylinositol-specific phospholipase C2 functions in auxin-modulated root development. Plant Cell Environ 42:1441–1457

    Article  CAS  PubMed  Google Scholar 

  • Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90:708–719

    Article  CAS  PubMed  Google Scholar 

  • Deng X, Yuan S, Cao H, Lam SM, Shui G, Hong Y, Wang X (2019) Phosphatidylinositol-hydrolyzing phospholipase C4 modulates rice response to salt and drought. Plant Cell Environ 42:536–548

    Article  CAS  PubMed  Google Scholar 

  • Duan P, Rao Y, Zeng D, Yang Y, Xu R, Zhang B, Dong G, Qian Q, Li Y (2014) SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice. Plant J 77:547–557

    Article  CAS  PubMed  Google Scholar 

  • Feng Z, Wu C, Wang C, Roh J, Zhang L, Chen J, Zhang S, Zhang H, Yang C, Hu J, You X, Liu X, Yang X, Guo X, Zhang X, Wu F, Terzaghi W, Kim SK, Jiang L, Wan J (2016) SLG controls grain size and leaf angle by modulating brassinosteroid homeostasis in rice. J Exp Bot 67:4241–4253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu JK (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao H, Jin M, Zheng XM, Chen J, Yuan D, Xin Y, Wang M, Huang D, Zhang Z, Zhou K, Sheng P, Ma J, Ma W, Deng H, Jiang L, Liu S, Wang H, Wu C, Yuan L, Wan J (2014) Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc Natl Acad Sci U S A 111:16337–16342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao H, Zheng XM, Fei G, Chen J, Jin M, Ren Y, Wu W, Zhou K, Sheng P, Zhou F, Jiang L, Wang J, Zhang X, Guo X, Wang JL, Cheng Z, Wu C, Wang H, Wan JM (2013) Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLoS Genet 9:e1003281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo T, Lu ZQ, Shan JX, Ye WW, Dong NQ, Lin HX (2020) ERECTA1 acts upstream of the OsMKKK10-OsMKK4-OsMPK6 cascade to control spikelet number by regulating cytokinin metabolism in rice. Plant Cell 32:2763–2779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722

    Article  CAS  PubMed  Google Scholar 

  • He Y, Wang S, Ding Y (2013) Identification of novel glutelin subunits and a comparison of glutelin composition between japonica and indica rice (Oryza sativa L.). J Cereal Sci 57:362–371

    Article  CAS  Google Scholar 

  • Heang D, Sassa H (2012) Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice. PLoS ONE 7:e31325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirayama T, Ohto C, Mizoguchi T, Shinozaki K (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A 92:3903–3907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hori K, Matsubara K, Yano M (2016) Genetic control of flowering time in rice: integration of Mendelian genetics and genomics. Theor Appl Genet 129:2241–2252

    Article  PubMed  Google Scholar 

  • Hu J, Wang Y, Fang Y, Zeng L, Xu J, Yu H, Shi Z, Pan J, Zhang D, Kang S, Zhu L, Dong G, Guo L, Zeng D, Zhang G, Xie L, Xiong G, Li J, Qian Q (2015) A rare allele of GS2 enhances grain size and grain yield in rice. Mol Plant 8:1455–1465

    Article  CAS  PubMed  Google Scholar 

  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  CAS  PubMed  Google Scholar 

  • Jia S, Xiong Y, Xiao P, Wang X, Yao J (2019) OsNF-YC10, a seed preferentially expressed gene regulates grain width by affecting cell proliferation in rice. Plant Sci 280:219–227

    Article  CAS  PubMed  Google Scholar 

  • Kim HY, Suh PG, Kim JI (2021) The role of phospholipase C in GABAergic inhibition and its relevance to epilepsy. Int J Mol Sci 22:3149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komiya R, Yokoi S, Shimamoto K (2009) A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136:3443–3450

    Article  CAS  PubMed  Google Scholar 

  • Li L, He Y, Wang Y, Zhao S, Chen X, Ye T, Wu Y, Wu Y (2015) Arabidopsis PLC2 is involved in auxin-modulated reproductive development. Plant J 84:04–515

    Article  Google Scholar 

  • Li L, Wang F, Yan P, Jing W, Zhang C, Kudla J, Zhang W (2017) A phosphoinositide-specific phospholipase C pathway elicits stress-induced Ca2+ signals and confers salt tolerance to rice. New Phytol 214:1172–1187

    Article  CAS  PubMed  Google Scholar 

  • Li N, Li Y (2016) Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33:23–32

    Article  PubMed  Google Scholar 

  • Li N, Xu R, Duan P, Li Y (2018) Control of grain size in rice. Plant Reprod 31:237–251

    Article  PubMed  Google Scholar 

  • Li N, Xu R, Li Y (2019) Molecular networks of seed size control in plants. Annu Rev Plant Biol 70:435–463

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Tong H, Xiao Y, Che R, Xu F, Hu B, Liang C, Chu J, Li J, Chu C (2015) Activation of big grain1 significantly improves grain size by regulating auxin transport in rice. Proc Natl Acad Sci U S A 112:11102–11107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Han R, Wu K, Zhang J, Ye Y, Wang S, Chen J, Pan Y, Li Q, Xu X, Zhou J, Tao D, Wu Y, Fu X (2018) G-protein βγ subunits determine grain size through interaction with MADS-domain transcription factors in rice. Nat Commun 27:852

    Article  Google Scholar 

  • Liu X, Cai WJ, Yin X, Yang D, Dong T, Feng YQ, Wu Y (2020) Two slender and crinkly leaf dioxygenases play an essential role in rice shoot development. J Exp Bot 71:1387–1401

    Article  CAS  PubMed  Google Scholar 

  • Lyu J, Wang D, Duan P, Liu Y, Huang K, Zeng D, Zhang L, Dong G, Li Y, Xu R, Zhang B, Huang X, Li N, Wang Y, Qian Q, Li Y (2020) Control of grain size and weight by the GSK2-LARGE1/OML4 pathway in rice. Plant Cell 32:1905–1918

    Article  PubMed  PubMed Central  Google Scholar 

  • Nishimura A, Aichi I, Matsuoka M (2006) A protocol for Agrobacterium-mediated transformation in rice. Nat Protoc 1:2796–2802

    Article  CAS  PubMed  Google Scholar 

  • Park SJ, Kim SL, Lee S, Je BI, Piao HL, Park SH, Kim CM, Ryu CH, Park SH, Xuan YH, Colasanti J, An G, Han CD (2008) Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J 56:1018–1029

    Article  CAS  PubMed  Google Scholar 

  • Peng Q, Zhu C, Liu T, Zhang S, Feng S, Wu C (2021) Phosphorylation of OsFD1 by OsCIPK3 promotes the formation of RFT1-containing florigen activation complex for long-day flowering in rice. Mol Plant 14:1135–1148

    Article  CAS  PubMed  Google Scholar 

  • Sagar S, Singh A (2021) Emerging role of phospholipase C mediated lipid signaling in abiotic stress tolerance and development in plants. Plant Cell Rep 40:2123–2133

    Article  CAS  PubMed  Google Scholar 

  • Segami S, Takehara K, Yamamoto T, Kido S, Kondo S, Iwasaki Y, Miura K (2017) Overexpression of SRS5 improves grain size of brassinosteroid-related dwarf mutants in rice (Oryza sativa L.). Breed Sci 67:393–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen W, Yao X, Ye T, Ma S, Liu X, Yin X, Wu Y (2018) Arabidopsis aspartic protease ASPG1 affects seed dormancy, seed longevity and seed germination. Plant Cell Physiol 59:1415–1431

    CAS  PubMed  Google Scholar 

  • Shim JS, Jang G (2020) Environmental signal-dependent regulation of flowering time in rice. Inter J Mol Sci 21:6155

    Article  CAS  Google Scholar 

  • Si L, Chen J, Huang X, Gong H, Luo J, Hou Q, Zhou T, Lu T, Zhu J, Shangguan Y, Chen E, Gong C, Zhao Q, Jing Y, Zhao Y, Li Y, Cui L, Fan D, Lu Y, Weng Q, Wang Y, Zhan Q, Liu K, Wei X, An K, An G, Han B (2016) OsSPL13 controls grain size in cultivated rice. Nat Genet 48:447–456

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Kanwar P, Pandey A, Tyagi AK, Sopory SK, Kapoor S, Pandey GK (2013) Comprehensive genomic analysis and expression profiling of phospholipase C gene family during abiotic stresses and development in rice. PLoS ONE 8:e62494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun C, Chen D, Fang J, Wang P, Deng X, Chu C (2014) Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways. Protein Cell 5:889–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun P, Zhang W, Wang Y, He Q, Shu F, Liu H, Wang J, Wang J, Yuan L, Deng H (2016) OsGRF4 controls grain shape, panicle length and seed shattering in rice. J Integr Plant Biol 58:836–847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun S, Wang L, Mao H, Shao L, Li X, Xiao J, Ouyang Y, Zhang Q (2018) A G-protein pathway determines grain size in rice. Nat Commun 9:851

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036

    Article  CAS  PubMed  Google Scholar 

  • Tsuji H, Taoka K, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol 14:45–52

    Article  CAS  PubMed  Google Scholar 

  • Wang X (2001) Plant phospholipases. Annu Rev Plant Physiol Plant Mol Biol 52:211–231

    Article  CAS  PubMed  Google Scholar 

  • Wei X, Jiao G, Lin H, Sheng Z, Shao G, Xie L, Tang S, Xu Q, Hu P (2017) GRAIN INCOMPLETE FILLING 2 regulates grain filling and starch synthesis during rice caryopsis development. J Integr Plant Biol 59:134–153

    Article  CAS  PubMed  Google Scholar 

  • Wu W, Liu X, Wang M, Meyer RS, Luo X, Ndjiondjop MN, Tan L, Zhang J, Wu J, Cai H, Sun C, Wang X, Wing RA, Zhu Z (2017) A single-nucleotide polymorphism causes smaller grain size and loss of seed shattering during African rice domestication. Nat Plants 3:17064

    Article  CAS  PubMed  Google Scholar 

  • Xia K, Wang B, Zhang J, Li Y, Yang H, Ren D (2017) Arabidopsis phosphoinositide-specific phospholipase C4 negatively regulates seedling salt tolerance. Plant Cell Environ 40:1317–1331

    Article  CAS  PubMed  Google Scholar 

  • Xiong W, Ye T, Yao X, Liu X, Ma S, Chen X, Chen ML, Feng YQ, Wu Y (2018) The dioxygenase GIM2 functions in seed germination by altering gibberellin production in Arabidopsis. J Integr Plant Biol 60:276–291

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Duan P, Yu H, Zhou Z, Zhang B, Wang R, Li J, Zhang G, Zhuang S, Lyu J, Li N, Chai T, Tian Z, Yao S, Li Y (2018) Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol Plant 11:860–873

    Article  CAS  PubMed  Google Scholar 

  • Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767

    Article  CAS  PubMed  Google Scholar 

  • Yang D, Liu X, Yin X, Dong T, Yu M, Wu Y (2021a) Rice non-specific phospholipase C6 is involved in mesocotyl elongation. Plant Cell Physiol 6:6

    Google Scholar 

  • Yang W, Wu K, Wang B, Liu H, Guo S, Guo X, Luo W, Sun S, Ouyang Y, Fu X, Chong K, Zhang Q, Xu Y (2021b) The RING E3 ligase CLG1 targets GS3 for degradation via the endosome pathway to determine grain size in rice. Mol Plant 14:1699–1713

    Article  CAS  PubMed  Google Scholar 

  • Yin X, Bai YL, Ye T, Yu M, Wu Y, Feng YQ (2022) Cinnamoyl coA:NADP oxidoreductase like 1 regulates abscisic acid response by modulating phaseic acid homeostasis in Arabidopsis thaliana. J Exp Bot 73:860–872

    Article  PubMed  Google Scholar 

  • Yin X, Liu X, Xu B, Lu P, Dong T, Yang D, Ye T, Feng YQ, Wu Y (2019) OsMADS18, a membrane-bound MADs-box transcription factor, modulates plant architecture and the ABA response in rice. J Exp Bot 70:3895–3909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida H, Nagato Y (2011) Flower development in rice. J Exp Bot 62:4719–4730

    Article  CAS  PubMed  Google Scholar 

  • Yu M, Cao C, Yin X, Liu X, Yang D, Gong C, Wang H, Wu Y (2021) The rice phosphoinositide-specific phospholipase C3 is involved in responses to osmotic stresses via modulating ROS homeostasis. Plant Sci 313:111087

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, van Wijk R, Zarza X, Shahbaz M, van Hooren M, Guardia A, Scuffi D, García-Mata C, Van den Ende W, Hoffmann-Benning S, Haring MA, Laxalt AM, Munnik T (2018) Knock-down of Arabidopsis PLC5 reduces primary root growth and secondary root formation while overexpression improves drought tolerance and causes stunted root hair growth. Plant Cell Physiol 59:2004–2019

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Wu Y, He Y, Wang Y, Xiao J, Li L, Wang Y, Chen X, Xiong W, Wu Y (2016) RopGEF2 is involved in ABA-suppression of seed germination and post-germination growth of Arabidopsis. Plant J 84:886–899

    Article  Google Scholar 

  • Zheng SZ, Liu YL, Li B, Shang ZL, Zhou RG, Sun DY (2012) Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J 69:689–700

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Zhu S, Cui S, Hou H, Wu H, Hao B, Cai L, Xu Z, Liu L, Jiang L, Wang H, Wan J (2021) Transcriptional and post-transcriptional regulation of heading date in rice. New Phytol 230:943–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu L, Dou L, Shang H, Li H, Yu J, Xiao G (2021) GhPIPLC2D promotes cotton fiber elongation by enhancing ethylene biosynthesis. Science 24:102199

    CAS  Google Scholar 

  • Zong W, Ren D, Huang M, Sun K, Feng J, Zhao J, Xiao D, Xie W, Liu S, Zhang H, Qiu R, Tang W, Yang R, Chen H, Xie X, Chen L, Liu YG, Guo J (2021) Strong photoperiod sensitivity is controlled by cooperation and competition among Hd1, Ghd7 and DTH8 in rice heading. New Phytol 229:1635–1649

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the members of the Wu Lab for their technical help and comments on this manuscript. We thank the ‘Large-scale Instrument and Equipment Sharing Foundation of Wuhan University’ for supporting the use of the instruments in the College of Life Sciences in Wuhan University. This work was supported by grants to Y.W. from the Major State Basic Research Program from the Ministry of Science and Technology of China (2013CB126900), and National Natural Science Foundation of China (31270333).

Funding

Ministry of Science and Technology of the People’s Republic of China, 2013CB126900, Yan Wu, National Natural Science Foundation of China, 31270333, Yan Wu

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yan Wu.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Communicated by Anastasios Melis.

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 (DOC 49,491 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, M., Huang, D., Yin, X. et al. The phosphoinositide-specific phospholipase C1 modulates flowering time and grain size in rice. Planta 256, 29 (2022). https://doi.org/10.1007/s00425-022-03941-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-022-03941-z

Keywords

Navigation