Acta Physiologiae Plantarum

, 42:19 | Cite as

Regulatory function of EARLI1-LIKE HYBRID PROLINE-RICH PROTEIN 1 in the floral transition of Arabidopsis thaliana

  • Zhen Du
  • Li Zhang
  • Na Tian
  • Meng-Xin Lu
  • Yan-Qin Ma
  • Jing-Wen Yao
  • Michael Schläppi
  • Zi-Qin XuEmail author
Original Article


The plasma membrane- and endoplasmic reticulum-localized proteins encoded by the EARLI1 (EARLY ARABIDOPSIS ALUMINUM INDUCED 1) subfamily of genes contain a signal peptide, a proline-rich domain and an eight-cysteine motif. We previously showed that knockdown of EARLI1 subfamily genes in the late-flowering background of Col-FRI-Sf2 accelerates flowering time, suggesting that EARLI1 genes participate in maintenance of vegetative growth and prevention of premature reproductive growth. We show here that ELHyPRP1 (EARLI1-LIKE HYBRID PROLINE-RICH PROTEIN 1, AT4G12490), a member of this subfamily, is induced by environmental factors such as cold and long-day photoperiod. Detailed analyses with RNA interference and overexpressing lines demonstrated that modulation of ELHyPRP1 can affect the expression of photoperiod, vernalization, gibberellin, age, and autonomous flowering pathway genes. When ELHyPRP1 and other EARLI1 subfamily genes were silenced by RNA interference, most genes participating in the promotion of flowering were activated, while suppressors of the floral transition were repressed. Downregulation of ELHyPRP1 leads to increased expression of the flowering time genes FT and SOC1, and enhanced circadian expression patterns of genes associated with the promotion of the floral transition. Together with the silencing of ELHyPRP1, the flowering repressor FLC and the GA signalling repressor RGA were inhibited. ELHyPRP1 transgenic tobacco plants displayed late-flowering phenotypes and their flowering time was remarkably delayed in comparison to the wild-type Qinyan 95 tobacco plants grown under long-day photoperiod. These results indicate that ELHyPRP1 may be involved in balancing biomass accumulation and seed proliferation.


ELHyPRP1 Flowering time Overexpression RNA interference Vegetative growth 



This work was supported by the National Natural Science Foundation of China (30870194, J1210063), the Research Project of Shaanxi Provincial Key Laboratory (15JS111), Graduate Research Project of Northwest University (YZZ15066) and the Opening Foundation of Key Laboratory of Resource Biology and Biotechnology in Western China (Northwest University), Ministry of Education.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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  1. Aukerman MJ, Lee I, Weigel D, Amasino RM (1999) The Arabidopsis flowering-time gene LUMINIDEPENDENS is expressed primarily in regions of cell proliferation and encodes a nuclear protein that regulates LEAFY expression. Plant J 18:195–203PubMedCrossRefPubMedCentralGoogle Scholar
  2. Blanco-Portales R, López-Raéz JA, Bellido ML, Moyano E, Dorado G, González-Reyes JA, Caballero JL, Muñoz-Blanco J (2004) A strawberry fruit-specific and ripening-related gene codes for a HyPRP protein involved in polyphenol anchoring. Plant Mol Biol 55:763–780PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bouton S, Viau L, Lelièvre E, Limami AM (2005) A gene encoding a protein with a proline-rich domain (MtPPRD1), revealed by suppressive subtractive hybridization (SSH), is specifically expressed in the Medicago truncatula embryo axis during germination. J Exp Bot 56:825–832PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9:1573–1584PubMedPubMedCentralGoogle Scholar
  5. Cecchini NM, Steffes K, Schläppi MR, Gifford AN, Greenberg JT (2015) Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nat Commun 6:7658PubMedCrossRefPubMedCentralGoogle Scholar
  6. Cecchini NM, Roychoudhry S, Speed DJ, Steffes K, Tambe A, Zodrow K, Konstantinoff K, Jung HW, Engle NL, Tschaplinski TJ, Greenberg JT (2019) Underground azelaic acid-conferred resistance to Pseudomonas syringae in Arabidopsis. Mol Plant Microbe Interact 32:86–94PubMedCrossRefPubMedCentralGoogle Scholar
  7. Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao QM, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43:421–427PubMedCrossRefPubMedCentralGoogle Scholar
  8. Chassot C, Nawrath C, Métraux JP (2007) Cuticular defects lead to full immunity to a major plant pathogen. Plant J 49:972–980PubMedCrossRefPubMedCentralGoogle Scholar
  9. Chaturvedi R, Venables B, Petros RA, Nalam V, Li M, Wang X, Takemoto LJ, Shah J (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J 71:161–172PubMedCrossRefPubMedCentralGoogle Scholar
  10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefGoogle Scholar
  11. Comai L, Moran P, Maslyar D (1990) Novel and useful properties of a chimeric plant promoter combining CaMV 35S and MAS elements. Plant Mol Biol 15:373–381PubMedCrossRefPubMedCentralGoogle Scholar
  12. Davila-Velderrain J, Martinez-Garcia JC, Alvarez-Buylla ER (2016) Dynamic network modelling to understand flowering transition and floral patterning. J Exp Bot 67:2565–2572PubMedCrossRefPubMedCentralGoogle Scholar
  13. Du Z, Xu D, Li L, Shi Y, Schläppi M, Xu ZQ (2012) Inhibitory effects of Arabidopsis EARLI1 against Botrytis cinerea and Bradysia difformis. Plant Cell Tiss Org 110:435–443CrossRefGoogle Scholar
  14. Dunoyer P, Thomas C, Harrison S, Revers F, Maule A (2004) A cysteine-rich plant protein potentiates Potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol 78:2301–2309PubMedPubMedCentralCrossRefGoogle Scholar
  15. Dvořáková L, Cvrčková F, Fischer L (2007) Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genom 8:412CrossRefGoogle Scholar
  16. Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550, 550.e1-2Google Scholar
  17. Gleave AP (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20:1203–1207PubMedCrossRefGoogle Scholar
  18. Huang G, Gong S, Xu W, Li P, Zhang D, Qin L, Li W, Li X (2011) GhHyPRP4, a cotton gene encoding putative hybrid proline-rich protein, is preferentially expressed in leaves and involved in plant response to cold stress. Acta Biochim Biophys Sin (Shanghai) 43:519–527CrossRefGoogle Scholar
  19. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91PubMedCrossRefGoogle Scholar
  20. Kazan K, Lyons R (2016) The link between flowering time and stress tolerance. J Exp Bot 67:47–60PubMedCrossRefPubMedCentralGoogle Scholar
  21. Kim DH, Sung S (2013) Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis. Plant Cell 25:454–469PubMedPubMedCentralCrossRefGoogle Scholar
  22. Liu F, Quesada V, Crevillén P, Bäurle I, Swiezewski S, Dean C (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28:398–407PubMedCrossRefPubMedCentralGoogle Scholar
  23. Mishra P, Panigrahi KC (2015) GIGANTEA - an emerging story. Front Plant Sci 6:8PubMedPubMedCentralCrossRefGoogle Scholar
  24. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15:473–497CrossRefGoogle Scholar
  25. Neto LB, de Oliveira RR, Wiebke-Strohm B, Bencke M, Weber RL, Cabreira C, Abdelnoor RV, Marcelino FC, Zanettini MH, Passaglia LM (2013) Identification of the soybean HyPRP family and specific gene response to Asian soybean rust disease. Genet Mol Biol 36:214–224PubMedPubMedCentralCrossRefGoogle Scholar
  26. Priyanka B, Sekhar K, Reddy VD, Rao KV (2010) Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol J 8:76–87PubMedCrossRefPubMedCentralGoogle Scholar
  27. Richter R, Bastakis E, Schwechheimer C (2013) Cross-repressive interactions between SOC1 and the GATAs GNC and GNL/CGA1 in the control of greening, cold tolerance, and flowering time in Arabidopsis. Plant Physiol 162:1992–2004PubMedPubMedCentralCrossRefGoogle Scholar
  28. Riedlmeier M, Ghirardo A, Wenig M, Knappe C, Koch K, Georgii E, Dey S, Parker JE, Schnitzler JP, Vlot AC (2017) Monoterpenes support systemic acquired resistance within and between plants. Plant Cell 29:1440–1459PubMedPubMedCentralCrossRefGoogle Scholar
  29. Seo PJ (2014) Recent advances in plant membrane-bound transcription factor research: emphasis on intracellular movement. J Integr Plant Biol 56:334–342PubMedCrossRefPubMedCentralGoogle Scholar
  30. Sheng J, D'Ovidio R, Mehdy MC (1991) Negative and positive regulation of a novel proline-rich protein mRNA by fungal elicitor and wounding. Plant J 1:345–354PubMedCrossRefPubMedCentralGoogle Scholar
  31. Shi Y, Zhang X, Xu ZY, Li L, Zhang C, Schläppi M, Xu ZQ (2011) Influence of EARLI1-like genes on flowering time and lignin synthesis of Arabidopsis thaliana. Plant Biol 13:731–739PubMedCrossRefPubMedCentralGoogle Scholar
  32. Sunmonu N, Kudo G (2014) How do sink and source activities influence the reproduction and vegetative growth of spring ephemeral herbs under different light conditions? J Plant Res 127:503–511PubMedCrossRefPubMedCentralGoogle Scholar
  33. Takeno K (2016) Stress-induced flowering: the third category of flowering response. J Exp Bot 67:4925–4934PubMedCrossRefPubMedCentralGoogle Scholar
  34. Vogel JP, Raab TK, Somerville CR, Somerville SC (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J 40:968–978PubMedCrossRefPubMedCentralGoogle Scholar
  35. Wanner LA, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 120:391–400PubMedPubMedCentralCrossRefGoogle Scholar
  36. Wilkosz R, Schläppi M (2000) A gene expression screen identifies EARLI1 as a novel vernalization-responsive gene in Arabidopsis thaliana. Plant Mol Biol 44:777–787PubMedCrossRefPubMedCentralGoogle Scholar
  37. Xu D, Huang X, Xu ZQ, Schläppi M (2011) The HyPRP gene EARLI1 has an auxiliary role for germinability and early seedling development under low temperature and salt stress conditions in Arabidopsis thaliana. Planta 234:565–577PubMedCrossRefPubMedCentralGoogle Scholar
  38. Yang CH, Chou ML (1999) FLD interacts with CO to affect both flowering time and floral initiation in Arabidopsis thaliana. Plant Cell Physiol 40:647–650PubMedCrossRefPubMedCentralGoogle Scholar
  39. Yang J, Zhang Y, Wang X, Wang W, Li Z, Wu J, Wang G, Wu L, Zhang G, Ma Z (2018) HyPRP1 performs a role in negatively regulating cotton resistance to V. dahliae via the thickening of cell walls and ROS accumulation. BMC Plant Biol 18:339PubMedPubMedCentralCrossRefGoogle Scholar
  40. Yeom SI, Seo E, Oh SK, Kim KW, Choi D (2012) A common plant cell-wall protein HyPRP1 has dual roles as a positive regulator of cell death and a negative regulator of basal defense against pathogens. Plant J 69:755–768PubMedCrossRefPubMedCentralGoogle Scholar
  41. Yeom M, Kim H, Lim J, Shin AY, Hong S, Kim JI, Nam HG (2014) How do phytochromes transmit the light quality information to the circadian clock in Arabidopsis? Mol Plant 7:1701–1704PubMedCrossRefPubMedCentralGoogle Scholar
  42. Yoo SC, Chen C, Rojas M, Daimon Y, Ham BK, Araki T, Lucas WJ (2013) Phloem long-distance delivery of FLOWERING LOCUS T (FT) to the apex. Plant J 75:456–468PubMedCrossRefPubMedCentralGoogle Scholar
  43. Yu K, Soares JM, Mandal MK, Wang C, Chanda B, Gifford AN, Fowler JS, Navarre D, Kachroo A, Kachroo P (2013) A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Rep 3:1266–1278PubMedCrossRefPubMedCentralGoogle Scholar
  44. Zhang Y, Schläppi M (2007) Cold responsive EARLI1 type HyPRPs improve freezing survival of yeast cells and form higher order complexes in plants. Planta 227:233–243PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2020

Authors and Affiliations

  1. 1.Key Laboratory of Resource Biology and Biotechnology in Western China (Ministry of Education), Shaanxi Provincial Key Laboratory of Biotechnology, College of Life SciencesNorthwest UniversityXi’anPeople’s Republic of China
  2. 2.Department of Biological SciencesMarquette UniversityMilwaukeeUSA

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