Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Blue and red light upregulate α-expansin 1 (EXPA1) in transgenic Brassica rapa and its overexpression promotes leaf and root growth in Arabidopsis

  • 35 Accesses

Abstract

Light quality and the cell-growth-related proteins called expansins (EXPs) are two crucial factors in plant growth and development. However, molecular insights into the light responses of EXPs and the influences of light-dependent EXP expression changes on plant growth and development remain scarce. A preliminary analysis using a cDNA microarray revealed that red, blue, violet, and far-red light emitting diode (LED) light exposure and dark periods differentially regulate the expression of 27 Brassica rapa EXPs (BrEXPs). The results indicated that photosynthetically significant red and blue light induce the expression of BrEXPA1, and these results were further confirmed using a semi-qRT-PCR assay. The identification of several light-responsive cis-regulatory elements in the BrEXP promoter sequences suggested that light signals were perceived through these promoter motifs to regulate the gene expression that eventually controls growth and development. To substantiate our hypothesis that the light-dependent regulation of EXPs modulates growth and development, we developed transgenic reporter lines of B. rapa expressing GUS under the BrEXPA1 promoter. A histochemical analysis showed that BrEXPA1-promoter-driven GUS activity was prominent in the leaves, radicles, lateral roots, and flowers of plants grown under monochromatic red or blue light. The biological functions of BrEXPA1 were further tested by overexpressing sense (OE-S) and antisense BrEXPA1 (OE-AS) transcripts in Arabidopsis. The OE-S lines displayed long radicles, wide leaves, and additional rosette leaves compared to the controls, whereas the OE-AS lines exhibited early bolting. Collectively, our results demonstrated the relationship between light and BrEXPs and also the light-dependent role of BrEXPA1 in growth regulation.

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

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

Data availability

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

References

  1. Abuqamar S, Ajeb S, Sham A, Enan MR, Iratni R (2013) A mutation in the expansin-like A2 gene enhances resistance to necrotrophic fungi and hypersensitivity to abiotic stress in Arabidopsis thaliana. Mol Plant Pathol 14:813–827

  2. Belfield EJ, Ruperti B, Roberts JA, Mcqueen-mason S (2005) Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. J Exp Bot 56:817–823

  3. Braidwood L, Breuer C, Sugimoto K (2014) My body is a cage: mechanisms and modulation of plant cell growth. New Phytol 201:388–402

  4. Castillo FM, Canales J, Claude A, Calderini DF (2018) Expansin genes expression in growing ovaries and grains of sunflower are tissue-specific and associate with final grain weight. BMC Plant Biol 18:327

  5. Chen F, Dahal P, Bradford KJ (2001) Two tomato expansin genes show divergent expression and localization in embryos during seed development and germination. Plant Physiol 127:928–936

  6. Chen Y, Han Y, Meng Z et al (2016) Overexpression of the wheat expansin gene TaEXPA2 improved seed production and drought tolerance in transgenic tobacco plants. PLoS One 11:1–24

  7. Chen L, Zou W, Fei C et al (2018) α-Expansin EXPA4 positively regulates abiotic stress tolerance but negatively regulates pathogen resistance in Nicotiana tabacum. Plant Cell Physiol 59:1–14

  8. Cho H-T, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788

  9. Choi D, Lee Y, Cho HT, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398

  10. Choi BS, Kim YJ, Markkandan K et al (2018) GW2 functions as an E3 ubiquitin ligase for rice. Int J Mol Sci 19:1904

  11. Cosgrove DJ (1998) Cell wall loosening by expansins. Plant Physiol 118:333–339

  12. Desfeux C, Clough SJ, Bent AF (2000) Female reproductive tissues are the primary target of agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol 123:895–904

  13. Dotto MC, Martínez GA, Civello PM (2006) Expression of expansin genes in strawberry varieties with contrasting fruit firmness. Plant Physiol Biochem 44:301–744

  14. Folta KM, Childers KS (2008) Light as a growth regulator: controlling plant biology with narrow-bandwidth solid-state lighting systems. HortScience 43:1957–1964

  15. Gil JF, Liebe S, Thiel H et al (2018) Massive up-regulation of LBD transcription factors and EXPANSINs highlights the regulatory programs of rhizomania disease. Mol Plant Pathol 19:2333–2348

  16. Golembeski GS, Imaizumi T (2015) Photoperiodic regulation of florigen function in Arabidopsis thaliana. Arabidopsis Book 13:e0178. https://doi.org/10.1199/tab.0178.10.1199/tab.0178

  17. Han Y, Chen Y, Yin S, Zhang M, Wang W (2015) Over-expression of TaEXPB23, a wheat expansin gene, improves oxidative stress tolerance in transgenic tobacco plants. J Plant Physiol 173:62–71

  18. Han T, Vaganov V, Cao S et al (2017) Improving “color rendering” of LED lighting for the growth of lettuce. Sci Rep 7:45944

  19. Heng W, Yang J, Hou Z et al (2018) Characterization and expression analysis of PbEXP genes in the epidermis of pear (Pyrus bretschneideri Rehd.). Plant Growth Regul 84:1–9

  20. Hong JK, Kim JS, Kim JA et al (2010) Identification and characterization of SHI family genes from Brassica rapa L. ssp. pekinensis. Genes Genomics 32:309–317

  21. Hu Y, Zhao Y (2016) Molecular basis for differential light responses in Arabidopsis stems and leaves. Proc Natl Acad Sci USA 113:5774–6113

  22. Hudson ME, Quail PH (2003) Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 133:1605–1616

  23. Johkan M, Shoji K, Goto F et al (2010) Blue light-emitting diode light irradiation of seedlings improves seedling quality and growth after transplanting in red leaf lettuce. HortScience 45:1809–1814

  24. Kaiser E (2019) Adding blue to red supplemental light increases biomass and yield of greenhouse-grown tomatoes, but only to an optimum. Front Plant Sci 9:2002

  25. Keuskamp DH, Sasidharan R, Vos I, Peeters AJ, Voesenek LA, Pierik R (2011) Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. Plant J 67:208–217

  26. Kim JA, Lee Y, Hong JK, Hong S (2013) Effects of light quality using LEDs on expression patterns in Brassica rapa seedlings. Korean J Hortic Sci Technol 31:607–616

  27. Krishnamurthy P, Muthusamy M, Kim JA, Lee SI (2019) Brassica rapa expansin-like B1 gene (BrEXLB1) regulate growth and development in transgenic Arabidopsis and elicits response to abiotic stresses. J Plant Biochem Biotechnol 28(4):437–446

  28. Kudo M, Kidokoro S, Yoshida T et al (2019) A gene-stacking approach to overcome the trade-off between drought stress tolerance and growth in Arabidopsis. Plant J 97:240–256

  29. Kuluev BR, Knyazev AB, Lebedev YP, Chemeris AV (2012) Morphological and physiological characteristics of transgenic tobacco plants expressing expansin genes: AtEXP10 from Arabidopsis and PnEXPA1 from poplar. Russ J Plant Physiol 59:97–104

  30. Lee D, Ahn JH, Song S et al (2003) Expression of an expansin gene is correlated with root elongation in soybean. Plant Physiol 131:985–997

  31. Lei XY, Wang QJ, Wang JW, Zheng LP (2017) Cloning and characterization of an expansin gene AbEXP from Achyranthes bidentata. Plant Growth Regul 83:479–487

  32. Liu TL, Newton L, Liu M et al (2016) A G-Box-like motif is necessary for transcriptional regulation by circadian pseudo-response regulators in Arabidopsis. Plant Physiol 170:528–539

  33. Ma Z, Li S, Zhang M (2010) Light intensity affects growth, photosynthetic capability, and total flavonoid accumulation of Anoectochilus plants. HortScience 45:863–867

  34. Ma N, Wang Y, Qiu S et al (2013) Overexpression of OsEXPA8 improves rice growth and root system architecture by facilitating cell extension. PLoS ONE 8:e75997.8

  35. Majda M, Robert S (2018) The role of auxin in cell wall expansion. Int J Mol Sci 19:951

  36. Marowa P, Ding A, Kong Y (2016) Expansins: roles in plant growth and potential applications in crop improvement. Plant Cell Rep 35:949–965

  37. McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578

  38. Muller B, Bourdais G, Reidy B et al (2007) Association of specific expansins with growth in maize leaves is maintained under environmental, genetic, and developmental sources of variation. Plant Physiol 143:278–290

  39. Ohtake N, Ishikura M, Suzuki H (2018) Continuous irradiation with alternating red and blue light enhances plant growth while keeping nutritional quality in lettuce. HortScience 53:1804–1809

  40. Pacifici E, Di Mambro R, Dello Ioio R, Costantino P, Sabatini S (2018) Acidic cell elongation drives cell differentiation in the Arabidopsis root. EMBO J 37:e99134

  41. Pedmale UV, Huang SS, Zander M et al (2016) Cryptochromes interact directly with PIFs to control plant growth in limiting blue light. Cell 164:233–245

  42. Ramakrishna P, Rance GA, Vu LD, Murphy E, Swarup K, Moirangthem K, Jorgensen B, van de Cotte B, Goh T, Lin Z, Voss U (2018) The expa1-1 mutant reveals a new biophysical lateral root organogenesis checkpoint. bioRxiv. https://doi.org/10.1101/249961

  43. Ramakrishna P, Ruiz P, Rance GA et al (2019) EXPANSIN A1-mediated radial swelling of pericycle cells positions anticlinal cell divisions during lateral root initiation. Proc Natl Acad Sci USA 116(17):8597–8602

  44. Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

  45. Rochange SF, Wenzel CL, Mcqueen-Mason SJ (2001) Impaired growth in transgenic plants over-expressing an expansin isoform. Plant Mol Biol 46:581–589

  46. Roman H, Girault T, Le Gourrierec J, Leduc N (2017) In silico analysis of 3 expansin gene promoters reveals 2 hubs controlling light and cytokinins response during bud outgrowth. Plant Signal Behav 12:489–509

  47. Ruan Y, Llewellyn DJ, Furbank RT (2001) The control of single-celled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13:47–60

  48. Shin JH, Jeong DH, Park MC, An G (2005) Characterization and transcriptional expression of the α-expansin gene family in rice. Mol Cells 20:210–218

  49. Sloan J, Backhaus A, Malinowski R et al (2009) Phased control of expansin activity during leaf development identifies a sensitivity window for expansin-mediated induction of leaf growth. Plant Physiol 151:1844–1854

  50. Sun T, Zhang Y, Chai T (2011) Cloning, characterization, and expression of the BjEXPA1 gene and its promoter region from Brassica juncea L. Plant Growth Regul 64:39–51

  51. Takemiya A, Inoue S, Doi M et al (2005) Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17:1120–1127

  52. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176

  53. Wang G, Gao Y, Wang J et al (2011) Overexpression of two cambium-abundant Chinese fir (Cunninghamia lanceolata) a-expansin genes ClEXPA1 and ClEXPA2 affect growth and development in transgenic tobacco and increase the amount of cellulose in stem cell walls. Plant Biotechnol J 9:486–502

  54. Zenoni S, Fasoli M, Tornielli GB et al (2011) Overexpression of PhEXPA1 increases cell size, modifies cell wall polymer composition and affects the timing of axillary meristem development in Petunia hybrida. New Phytol 191:662–677

  55. Zhang X, Wei P, Xiong Y et al (2011) Overexpression of the Arabidopsis a-expansin gene AtEXPA1 accelerates stomatal opening by decreasing the volumetric elastic modulus. Plant Cell Rep 30:27–36

  56. Zhang Y, Kaiser E, Zhang Y et al (2018) Red/blue light ratio strongly affects steady-state photosynthesis, but hardly affects photosynthetic induction in tomato (Solanum lycopersicum). Physiol Plant. https://doi.org/10.1111/ppl.12876

  57. Zhen S, van Iersel MW (2017) Far-red light is needed for efficient photochemistry and photosynthesis. J Plant Physiol 209:115–122

  58. Zheng L, Van Labeke M (2017) Long-term effects of red- and blue-light emitting diodes on leaf anatomy and photosynthetic efficiency of three ornamental pot plants. Front Plant Sci 8:917

  59. Zhou P, Zhu Q, Xu J et al (2011) Cloning and characterization of a gene, AsEXP1, encoding expansin proteins inducible by heat stress and hormones in creeping bentgrass. Crop Sci 51:333–341

  60. Zhou J, Xie J, Liao H, Wang X (2014) Overexpression of β-expansin gene GmEXPB2 improves phosphorus efficiency in soybean. Physiol Plant 150:194–204

Download references

Acknowledgements

This work was supported by the Rural Development Administration (Korea) through the Rural Program for Agricultural Science and Technology Development (Project No. PJ01495701) and the New Breeding Technology center (Project No. PJ01492901).

Author information

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by SIL and MM. MM and SIL wrote the manuscript, which was reviewed by JAK and M-JJ. All authors read and approved the final manuscript.

Correspondence to Soo In Lee.

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.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Muthusamy, M., Kim, J.A., Jeong, M. et al. Blue and red light upregulate α-expansin 1 (EXPA1) in transgenic Brassica rapa and its overexpression promotes leaf and root growth in Arabidopsis. Plant Growth Regul (2020). https://doi.org/10.1007/s10725-020-00588-2

Download citation

Keywords

  • Light-responsive promoter motifs
  • Expansins
  • Red and blue light responses
  • Brassica rapa
  • EXPA1
  • Microarray
  • Transgenic reporter lines