Skip to main content
Log in

The role of phytochrome-mediated gibberellic acid signaling in the modulation of seed germination under low light stress in rice (O. sativa L.)

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Seed germination plays cardinal roles in seedling establishment and their successive growth. However, seed germination is retarded by far-red (FR) enrichment under low light stress, and the inhibitory signalling mechanism remains ambiguous. Our results indicated that low light treatment, both in the open and growth chamber conditions, inhibits rice seed germination by decreasing the gibberellin (GA) contents. To explore the mechanism of GA-deficiency under low light stress, differential expression profiling of GA-anabolic, -catabolic, ABA -anabolic, -catabolic, and SLR1 was investigated, revealing that expression of ABA- anabolic, GA-catabolic genes and SLR1 was upregulated with a simultaneous downregulation of ABA-catabolic and GA-anabolic genes under low light treatment. These results suggested that FR-induced GA inadequacy is resulted by upregulation of SLR1 and GA-catabolism genes consequently increase DELLA that further subsided GA-responses in the germinating rice seeds. Moreover, we provided evidence that FR-induced GA inadequacy demotes rice seed germination by decreasing amylase activity, eventually decreasing the carbohydrate solubilization in the germinating seeds. Finally, we suggest that under low light stress, due to a retarded conversion of phytochrome A to their bioactive form, the ABA-catabolic genes were eventually upregulated with a simultaneous downregulation of GA-anabolic genes. Consequently, a lower GA pool fails to leverage the GA-dependent DELLA degradation, further shutting down the expected GA responses that reduce germination efficiency under FR-enriched light.

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
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Appleford NE, Wilkinson MD, Ma Q, Evans DJ, Stone MC, Pearce SP, Powers SJ, Thomas SG, Jones HD, Phillips AL, Hedden P, Lenton JR (2007) Decreased shoot stature and grain α-amylase activity following ectopic expression of a gibberellin 2-oxidase gene in transgenic wheat. J Exp Bot 58(12):3213–3226

    Article  CAS  PubMed  Google Scholar 

  • Atzorn R, Weiler EW (1983) The role of endogenous gibberellins in the formation of α-amylase by aleurone layers of germinating barley caryopses. Planta 159(4):289–299

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Roychoudhury A (2019) The regulatory signaling of gibberellin metabolism and its crosstalk with phytohormones in response to plant abiotic stresses. Plant signaling molecules. Woodhead Publishing, pp 333–339

  • Bardhan S, Panigrahi KCS (2018) Mechanisms involved in response to shade in rice. A review. In: Proceedings of the International Conference on Plant Developmental Biology. Cambridge Scholars Publishing, pp 3–15

  • Beck E, Ziegler P (1989) Biosynthesis and degradation of starch in higher plants. Annu Rev Plant Physiol Plant Mol Biol 40(1):95–117

    Article  CAS  Google Scholar 

  • Bose B, Kumar M, Singhal RK, Mondal S (2018) Impact of seed priming on the modulation of physico-chemical and molecular processes during germination, growth, and development of crops. In: Amitava Rakshit A, Singh HB (eds) Advances in seed priming. Springer, Singapore, pp 23–40

    Google Scholar 

  • Botto JF, Sanchez RA, Whitelam GC, Casal JJ (1996) Phytochrome A mediates the promotion of seed germination by very low fluences of light and canopy shade light in Arabidopsis. Plant Physiol 110(2):439–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao D, Hussain A, Cheng H, Peng J (2005) Loss of function of four DELLA genes leads to light-and gibberellin-independent seed germination in Arabidopsis. Planta 223(1):105–113

    Article  CAS  PubMed  Google Scholar 

  • Cordeiro AM, Figueiredo DD, Tepperman J, Borba AR, Lourenço T, Abreu IA, Ouwerkerk PBF, Quail PH, Oliveira MM, Saibo NJM (2016) Rice phytochrome-interacting factor protein OsPIF14 represses OsDREB1B gene expression through an extended N-box and interacts preferentially with the active form of phytochrome B. Biochim Biophys Acta Gene Regul Mech 1859(2):393–404

    Article  CAS  Google Scholar 

  • Cornea-Cipcigan M, Pamfil D, Sisea CR, Mărgăoan R (2020) Gibberellic acid can improve seed germination and ornamental quality of selected cyclamen species grown under short and long days. Agronomy 10(4):516

    Article  CAS  Google Scholar 

  • Cui K, Peng S, Xing Y, Xu C, Yu S, Zhang Q (2002) Molecular dissection of seedling-vigor and associated physiological traits in rice. Theor Appl Genet 105(5):745–753

    Article  CAS  PubMed  Google Scholar 

  • Dey P, Datta D, Pattnaik D, Dash D, Saha D, Panda D, Singhal RK (2021) Physiological, biochemical, and molecular adaptation mechanisms of photosynthesis and respiration under challenging environments. Plant perspectives to global climate changes. Academic Press, Cambridge, pp 79–100

    Google Scholar 

  • El-Keblawy A, Gairola S (2017) Dormancy regulating chemicals alleviate innate seed dormancy and promote germination of desert annuals. J Plant Growth Regul 36(2):300–311

    Article  CAS  Google Scholar 

  • Fisher RA (1936) The use of multiple measurements in taxonomic problems. Ann Eugen 7:179–188

    Article  Google Scholar 

  • Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61(1):11–24

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Li C, Mohan H, Probst N (2013) Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorable conditions. Plant Cell Rep 32(7):1007–1016

    Article  CAS  PubMed  Google Scholar 

  • Graham HD, Thomas LB (1961) Rapid, simple colorimetric method for the determination of micro quantities of gibberellic acid. J Pharm Sci 50(1):44–48

    Article  CAS  PubMed  Google Scholar 

  • Hammer O, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Hisamatsu T, King RW (2008) The nature of floral signals in Arabidopsis. II. Roles for FLOWERING LOCUS T (FT) and gibberellin. J Exp Bot 59(14):3821–3829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, López-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M, Pradervand S, Xenarios I, Fankhauser C (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signalling. Plant J 71:699–711

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143(4):1467–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8(3):217–230

    Article  CAS  PubMed  Google Scholar 

  • Karrer E, Chandler JM, Foolad MR, Rodriguez RL (1993) Seedling vigor is correlated to the expression of one member of the rice α-amylase multigene family. Euphytica 66(3):163–169

    Article  Google Scholar 

  • Kim ST, Kang SY, Wang Y, Kim SG, Hwang DH, Kang KY (2008) Analysis of embryonic proteome modulation by GA and ABA from germinating rice seeds. Proteomic 8(17):3577–3587

    Article  CAS  Google Scholar 

  • Kim H, Hwang H, Hong JW, Lee YN, Ahn IP, Yoon IS, Yoo SD, Lee S, Kim BG (2012) A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. J Exp Bot 63(2):1013–1024

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Sahoo U, Baisakha B, Okpani OA, Ngangkham U, Parameswaran C, Basak N, Kumar G, Sharma SG (2018) Resistant starch could be decisive in determining the glycemic index of rice cultivars. J Cereal Sci 79:348–353

    Article  CAS  Google Scholar 

  • Kumar A, Panda D, Mohanty S, Biswal M, Dey P, Dash M, Sah RP, Kumar S, Baig MJ, Behera L (2020) Role of sedoheptulose-1, 7 bisphosphatase in low light tolerance of rice (Oryza sativa L.). Physiol Mol Biol Plant 26:2465–2485

    Article  CAS  Google Scholar 

  • Meng Y, Chen F, Shuai H, Luo X, Ding J, Tang S, Yang W (2016) Karrikins delay soybean seed germination by mediating abscisic acid and gibberellin biogenesis under shaded conditions. Sci Rep 6(1):1–12

    Google Scholar 

  • Mo W, Tang W, Jing Y, Bu Q, Lin R (2020) PHYTOCHROME-INTERACTING FACTOR-LIKE14 and SLENDER RICE1 interaction controls seedling growth under salt stress. Plant Physiol 184(1):506–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohanty S, Donde R, Das S, Panda D, Mishra B, Pradhan SK, Behera L (2021) Utilization of genetic diversity and population structure to reveal prospective drought-tolerant donors in rice. Gene Rep 23:101151

    Article  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32(7):959–970

    Article  CAS  PubMed  Google Scholar 

  • Naredo MEB, Juliano AB, Lu BR, De Guzman F, Jackson MT (1998) Responses to seed dormancy-breaking treatments in rice species (Oryza sativa L.). Seed Sci Technol 26:675–690

    Google Scholar 

  • Nayak SK, Janardhan KV, Murty KS (1978) Photosynthetic efficiency of rice as influenced by light intensity and quality. Indian J Plant Physiol 21(1):48–52

    Google Scholar 

  • Nayak L, Panda D, Dash GK, Lal MK, Swain P, Baig MJ, Kumar A (2021) A chloroplast Glycolate catabolic pathway bypassing the endogenous photorespiratory cycle enhances photosynthesis, biomass and yield in rice (Oryza sativa L.). Plant Sci 314:111103

    Article  PubMed  Google Scholar 

  • Oh E, Yamaguchi S, Kamiya Y, Bae G, Chung WI, Choi G (2006) Light activates the degradation of PIL5 protein to promote seed germination through gibberelin in Arabidopsis. Plant J 47(1):124–139

    Article  CAS  PubMed  Google Scholar 

  • Panda D (2014) Development of genetically engineered plant photoreceptors for generating crop plants with novel agronomic traits. Int J Genet Eng Biotechnol 5:93–102

    Google Scholar 

  • Panda D, Biswal M, Mohanty S, Dey P, Swain A, Behera D, Baig MJ, Kumar A, Sah RP, Tripathy BC, Behera L (2020) Contribution of phytochrome a in the regulation of sink capacity starch biosynthesis, grain quality, grain yield and related traits in rice. Plant Archiv 20(1):1179–1194

    Google Scholar 

  • Perata P, Guglielminetti L, Alpi A (1997) Mobilization of endosperm reserves in cereal seeds under anoxia. Annal Bot 79(1):49–56

    Article  CAS  Google Scholar 

  • Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L (2008) The gibberellic acid signalling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20(10):2729–2745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piskurewicz U, Turečková V, Lacombe E, Lopez-Molina L (2009) Far-red light inhibits germination through DELLA-dependent stimulation of ABA synthesis and ABI3 activity. EMBO J 28(15):2259–2271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi L, Liu S, Li C, Fu J, Jing Y, Cheng J, Li H, Zhang D, Wang X, Dong X, Han R, Li B, Zhang Y, Li Z, Terzaghi W, Song C-P, Lin R, Gong Z, Li J (2020) PHYTOCHROME-INTERACTING FACTORS interact with the ABA receptors PYL8 and PYL9 to orchestrate ABA signaling in darkness. Mol Plant 13(3):414–430

    Article  CAS  PubMed  Google Scholar 

  • Ravindran P, Kumar PP (2019) Regulation of seed germination: the involvement of multiple forces exerted via gibberellic acid signalling. Mol Plant 12(1):24–26

    Article  CAS  PubMed  Google Scholar 

  • Rood SB, Larsen KM (1988) Gibberellins, amylase, and the onset of heterosis in maize seedlings. J Exp Bot 39(2):223–233

    Article  CAS  Google Scholar 

  • Roy A, Sahoo D, Tripathy BC (2013) Involvement of phytochrome A in suppression of photomorphogenesis in rice seedling grown in red light. Plant Cell Environ 36(12):2120–2134

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signaling. Curr Opin Plant Biol 12(1):57–62

    Article  CAS  PubMed  Google Scholar 

  • Sekhar S, Panda D, Kumar J, Mohanty N, Biswal M, Baig MJ, Kumar A, Umakanta N, Samantaray S, Pradhan SK, Shaw BP, Swain P, Behera L (2019) Comparative transcriptome profiling of low light tolerant and sensitive rice varieties induced by low light stress at active tillering stage. Sci Rep 9(1):1–14

    Article  CAS  Google Scholar 

  • Sheerin DJ, Hiltbrunner A (2017) Molecular mechanisms and ecological function of far-red light signalling. Plant Cell Environ 40(11):2509–2529

    Article  CAS  PubMed  Google Scholar 

  • Shichijo C, Katada K, Tanaka O, Hashimoto T (2001) Phytochrome A-mediated inhibition of seed germination in tomato. Planta 213(5):764–769

    Article  CAS  PubMed  Google Scholar 

  • Shu K, Zhou W, Chen F, Luo X, Yang W (2018) Abscisic acid and gibberellin antagonistically mediate plant development and abiotic stress responses. Front Plant Sci 9:416

    Article  PubMed  PubMed Central  Google Scholar 

  • Sineshchekov V, Koppel L, Riemann M, Nick P (2020) Phytochrome a and its functional manifestations in etiolated and far-red light-grown seedlings of the wild-type rice and its hebiba and cpm2 mutants deficient in the defence-related phytohormone jasmonic acid. Photochem Photobiol 97(2):335–342

    Article  PubMed  Google Scholar 

  • Takano M, Inagaki N, Xie X, Yuzurihara N, Hihara F, Ishizuka T, Shinomura T (2005) Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 17(12):3311–3325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur S, Asthir B, Kaur G, Kalia A, Sharma A (2021) Zinc oxide and titanium dioxide nanoparticles influence heat stress tolerance mediated by antioxidant defense system in wheat. Cereal Res Commun 21(7):1–12

    Google Scholar 

  • Todaka D, Nakashima K, Maruyama K, Kidokoro S, Osakabe Y, Ito Y, Matsukura S, Fujita Y, Yoshiwara K, Ohme-Takagi M, Kojima M, Sakakibara H, Shinozaki K, Yamaguchi-Shinozaki K (2012) Rice phytochrome-interacting factor-like protein OsPIL1 functions as a key regulator of internode elongation and induces a morphological response to drought stress. Proc Natl Acad Sci 109(39):15947–15952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toyomasu T, Kawaide H, Mitsuhashi W, Inoue Y, Kamiya Y (1998) Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. Plant Physiol 118(4):1517–1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuan PA, Kumar R, Rehal PK, Toora PK, Ayele BT (2018) Molecular mechanisms underlying abscisic acid/gibberellin balance in the control of seed dormancy and germination in cereals. Front Plant Sci 9:668–672

    Article  PubMed  PubMed Central  Google Scholar 

  • Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I, Matsuoka M (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19(7):2140–2155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaistij FE, Barros-Galvão T, Cole AF, Gilday AD, He Z, Li Y, Harvey D, Larson TR, Graham IA (2018) MOTHER-OF-FT-AND-TFL1 represses seed germination under far-red light by modulating phytohormone responses in Arabidopsis thaliana. Proc Natl Acad Sci 115(33):8442–8447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vishal B, Kumar PP (2018) Regulation of seed germination and abiotic stresses by gibberellins and abscisic acid. Front Plant Sci 9:838

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie Y, Liu Y, Wang H, Ma X, Wang B, Wu G, Wang H (2017) Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis. Nat Commun 8(1):1–11

    Article  Google Scholar 

  • Yamauchi Y, Takeda-Kamiya N, Hanada A, Ogawa M, Kuwahara A, Seo M, Yamaguchi S (2007) Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant Cell Physiol 48(3):555–561

    Article  CAS  PubMed  Google Scholar 

  • Yan Y, Li C, Dong X, Li H, Zhang D, Zhou Y, Jiang B, Peng J, Qin X, Cheng J, Wang X, Song P, Qi l, Zheng Y, Li B, Terzaghi W, Yang S, Gou Y, Li J, (2020) MYB30 is a key negative regulator of Arabidopsis photomorphogenic development that promotes PIF4 and PIF5 protein accumulation in the light. Plant Cell 32(7):2196–2215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang G, Zhang Q (1990) Polymorphisms of α-amylase activity in barley landraces and cultivars from China. Euphytica 48(3):245–251

    Article  CAS  Google Scholar 

  • Yano K, Aya K, Hirano K, Ordonio RL, Ueguchi-Tanaka M, Matsuoka M (2015) Comprehensive gene expression analysis of rice aleurone cells: probing the existence of an alternative gibberellin receptor. Plant Physiol 167(2):531–544

    Article  CAS  PubMed  Google Scholar 

  • Yu SM (1999) Cellular and genetic responses of plants to sugar starvation. Plant Physiol 121(3):687–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Tong H, Bai N, Liu M, Xiao T, Xue W (2020) Phytohormone dynamics in developing endosperm influence rice grain shape and quality. J Int Plant Biol 62(10):1625–1637

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The financial assistance received from the Indian Council of Agricultural Research, New Delhi, India is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Contributions

DP and SM equally contributed to work in conceptualization, design, Material preparation, data collection, writing and statistical analysis of the work. SD done the lab work and data entry. RPS helped in data curation and visualization. AK helped in Biochemical study. LB has done the Investigation, validation, reviewing, editing and finalization of the manuscript. MJB and BCT guided in whole manuscript preparation and the physiological work.

Corresponding author

Correspondence to Lambodar Behera.

Ethics declarations

Conflict of interest

The authors did not receive support from any organization for the submitted work. The authors have no competing interests to declare that are relevant to the content of this article. There is no conflict of interest among the authors regarding the authorship of this manuscript.

Additional information

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 (DOCX 2771 kb)

Supplementary file2 (XLSX 105 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Panda, D., Mohanty, S., Das, S. et al. The role of phytochrome-mediated gibberellic acid signaling in the modulation of seed germination under low light stress in rice (O. sativa L.). Physiol Mol Biol Plants 28, 585–605 (2022). https://doi.org/10.1007/s12298-022-01167-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-022-01167-7

Keywords

Navigation