Abstract
Cryptochrome 2 (CRY2) perceives blue/UV-A light and regulates photomorphogenesis in plants. However, besides Arabidopsis, CRY2 has been functionally characterized only in native species of japonica rice and tomato. In the present study, the BnCRY2a, generating a relatively longer cDNA and harboring an intron in its 5′UTR, has been characterized in detail. Western blot analysis revealed that BnCRY2a is light labile and degraded rapidly by 26S proteasome when seedlings are irradiated with blue light. For functional analysis, BnCRY2a was over-expressed in Brassica juncea, a related species more amenable to transformation. The BnCRY2a over-expression (BnCRY2aOE) transgenics developed short hypocotyl and expanded cotyledons, accumulated more anthocyanin in light-grown seedlings, and displayed early flowering on maturity. Early flowering in BnCRY2aOE transgenics was coupled with the up-regulation of many flowering-related genes such as FT. The present study also highlights the differential light sensitivity of cry1 and cry2 in controlling hypocotyl elongation growth in Brassica. BnCRY2aOE seedlings developed much shorter hypocotyl under the low-intensity of blue light, while BnCRY1OE seedling hypocotyls were shorter under the high-intensity blue light, compared to untransformed seedlings.
Key message
Brassica napus (2n = 38, AACC) is an allotetraploid derived from cross-hybridization of B. rapa (2n = 20, AA) and B. oleracea (2n = 18, CC), followed by chromosome doubling. It is an important oilseed crop, and therefore, efforts are being made to enhance its agronomic traits. Early flowering is one of the essential agronomic traits which the breeders have long targeted in order to shorten the life cycle of Brassica. Early flowering along with delayed maturity, and high leaf area index lead to increase in seed yield. Due to the problem of global warming, high temperature during the terminal stage of a crop can result in significant yield loss as high temperature has a negative effect on bud formation to silique development stage. In this research article, we have reported that overexpression of BnCRY2a in Brassica juncea results in early flowering. This opens the door for making early flowering variety of Brassica napus a reality without any yield penalty. In-depth analysis of the pathway BnCRY2a follows to cause early flowering phenotype will significantly enhance our knowledge on the mechanism of flowering in oilseed crop plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The microarray data has been uploaded in Gene Expression Omnibus (GEO) database and its accession number is GSE81459.
References
Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166
Ahmad M, Jarillo JA, Cashmore AR (1998a) Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell 10:197–207. https://doi.org/10.1105/tpc.10.2.197
Ahmad M, Jarillo JA, Smirnova O, Cashmore AR (1998b) The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome a in vitro. Mol Cell 1:939–948. https://doi.org/10.1016/S1097-2765(00)80094-5
Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1:213–222. https://doi.org/10.1016/S1097-2765(00)80022-2
Arundhati A, Feiler H, Traas J, Zhang H, Lunness PA, Doonan JH (1995) A novel Arabidopsis type 1 protein phosphatase is highly expressed in male and female tissues and functionally complements a conditional cell cycle mutant of Aspergillus. Plant J 7:823–834. https://doi.org/10.1046/j.1365-313X.1995.07050823.x
Banerjee R, Batschauer A (2005) Plant blue-light receptors. Planta 220:498–502. https://doi.org/10.1007/s00425-004-1418-z
Bayer PE, Hurgobin B, Golicz AA, Chan CKK, Yuan Y, Lee HT, Renton M, Meng J, Li R, Long Y, Zou J, Bancroft I, Chalhoub B, King GJ, Batley J, Edwards D (2017) Assembly and comparison of two closely related Brassica napus genomes. Plant Biotechnol J 15:1602–1610. https://doi.org/10.1111/pbi.12742
Ben-Gera H, Dafna A, Alvarez JP, Bar M, Mauerer M, Ori N (2016) Auxin-mediated lamina growth in tomato leaves is restricted by two parallel mechanisms. Plant J 86:443–457. https://doi.org/10.1111/tpj.13188
Bharti AK, Khurana JP (1997) Mutants of Arabidopsis as tools to understand the regulation of phenylpropanoid pathway and UVB protection mechanisms. Photochem Photobiol 65:765–776. https://doi.org/10.1111/j.1751-1097.1997.tb01923.x
Bhatnagar A, Singh S, Khurana JP, Burman N (2020) HY5-COP1: the central module of light signaling pathway. J Plant Biochem Biotechnol 29:590–610. https://doi.org/10.1007/s13562-020-00623-3
Buschmann H, Fabri CO, Hauptmann M, Hutzler P, Laux T, Lloyd CW, Schaffner A (2004) Helical growth of the arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein henrik. Curr Biol 14:1515–1521
Busk PK, Pagès M (1997) Microextraction of nuclear proteins from single maize embryos. Plant Mol Biol Rep 15:371–376. https://doi.org/10.1023/A:1007428802474
Carles CC, Choffnes-Inada D, Reville K, Lertpiriyapong K, Fletcher JC (2005) ULTRAPETALA1 encodes a SAND domain putative transcriptional regulator that controls shoot and floral meristem activity in Arabidopsis. Development 132:897–911. https://doi.org/10.1242/dev.01642
Cashmore AR, Jarillo JA, Wu YJ, Liu D (1999) Cryptochromes: blue light receptors for plants and animals. Science 284:760–765. https://doi.org/10.1126/science.284.5415.760
Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science 345:950–953. https://doi.org/10.1126/science.1253435
Chatterjee M, Sharma P, Khurana JP (2006) Cryptochrome 1 from Brassica napus is up-regulated by blue light and controls hypocotyl/stem growth and anthocyanin accumulation. Plant Physiol 141:61–74. https://doi.org/10.1104/pp.105.076323
Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ, O’Hara A, Kelly SM, Hothorn M, Smith BO, Hitomi K, Jenkins GI, Getzoff ED (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335(6075):1492–1496. https://doi.org/10.1126/science.1218091
Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38:332–347. https://doi.org/10.1111/j.1365-313X.2004.02052.x
Das Gupta M, Aggarwal P, Nath U (2014) CINCINNATA in Antirrhinum majus directly modulates genes involved in cytokinin and auxin signaling. New Phytol 204:901–912. https://doi.org/10.1111/nph.12963
Dornelas MC, Lejeune B, Dron M, Kreis M (1998) The Arabidopsis SHAGGY-related protein kinase (ASK) gene family: structure, organization and evolution. Gene 212:249–257. https://doi.org/10.1016/S0378-1119(98)00147-4
Dornelas MC, Van Lammeren AAM, Kreis M (2000) Arabidopsis thaliana SHAGGY-related protein kinases (AtSK11 and 12) function in perianth and gynoecium development. Plant J 21:419–429. https://doi.org/10.1046/j.1365-313X.2000.00691.x
Duek PD, Fankhauser C (2003) HFR1, a putative bHLH transcription factor, mediates both phytochrome A and cryptochrome signalling. Plant J 34:827–836. https://doi.org/10.1046/j.1365-313X.2003.01770.x
El-Din El-Assal S, Alonso-Blanco C, Peeters AJM, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29:435–440. https://doi.org/10.1038/ng767
Fantini E, Sulli M, Zhang L, Aprea G, Jiménez-Gómez JM, Bendahmane A, Perrotta G, Giuliano G, Facella P (2019) Pivotal roles of cryptochromes 1a and 2 in tomato development and physiology 1[OPEN]. Plant Physiol 179:732–748. https://doi.org/10.1104/pp.18.00793
Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000) The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development 127:4443–4453. https://doi.org/10.1242/dev.127.20.4443
Gao Y, Li J, Strickland E, Hua S, Zhao H, Chen Z, Qu L, Deng XW (2004) An arabidopsis promoter microarray and its initial usage in the identification of HY5 binding targets in vitro. Plant Mol Biol 54:683–699. https://doi.org/10.1023/B:PLAN.0000040898.86788.59
Gazave E, Lapébie P, Richards GS, Brunet F, Ereskovsky AV, Degnan BM, Borchiellini C, Vervoort M, Renard E (2009) Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol Biol 9:1–27. https://doi.org/10.1186/1471-2148-9-249
Giliberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, Bramley PM, Fiore A, Tavazza M, Giuliano G (2005) Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development flowering time, and fruit antioxidant content. Plant Physiol 137(1):199–208
Gregis V, Sessa A, Colombo L, Kater MM (2006) AGL24, SHORT VEGETATIVE PHASE, and APETALA1 redundantly control AGAMOUS during early stages of flower development in Arabidopsis. Plant Cell 18:1373–1382. https://doi.org/10.1105/tpc.106.041798
Gregis V, Sessa A, Dorca-Fornell C, Kater MM (2009) The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. Plant J 60:626–637. https://doi.org/10.1111/j.1365-313X.2009.03985.x
Guo H, Yang H, Mockler TC, Lin C (1998) Regulation of flowering time by Arabidopsis photoreceptors. Science 279:1360–1363. https://doi.org/10.1242/dev.02340
Guo H, Duong H, Ma N, Lin C (1999) The Arabidopsis blue light receptor cryptochrome 2 is a nuclear protein regulated by a blue light-dependent post-transcriptional mechanism. Plant J 19:279–287. https://doi.org/10.1046/j.1365-313X.1999.00525.x
Habekotté B (1997) Options for increasing seed yield of winter oilseed rape (Brassica napus L.):a simulation study. Field Crops Res 54:109–126. https://doi.org/10.1016/S0378-4290(97)00041-5
Hirose F, Shinomura T, Tanabata T, Shimada H, Takano M (2006) Involvement of rice cryptochromes in de-etiolation responses and flowering. Plant Cell Physiol 47:915–925. https://doi.org/10.1105/tpc.113.121830
Hudson M, Ringli C, Boylan MT, Quail PH (1999) The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev 13:2017–2027. https://doi.org/10.1101/gad.13.15.2017
Imaizumi T, Kanegae T, Wada M (2000) Cryptochrome nucleocytoplasmic distribution and gene expression are regulated by light quality in the fern Adiantum capillus-veneris. Plant Cell 12:81–95. https://doi.org/10.2307/3871031
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 143:1467–1483. https://doi.org/10.1104/pp.106.091900
Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim WY, Van Oosten M, Hyun Y, Somers DE, Lee I, Yun DJ, Bressan RA, Hasegawa PM (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J 53:530–540. https://doi.org/10.1111/j.1365-313X.2007.03359.x
Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66. https://doi.org/10.1016/S0070-2153(10)91002-8
Kanegae T, Wada M (1998) Isolation and characterization of homologues of plant blue-light photoreceptor (cryptochrome) genes from the fern Aliantum capillus-veneris. Mol Gen Genet 259:345–353. https://doi.org/10.1007/s004380050821
Khurana JP, Chatterjee M, Sharma P, Kumar D (2009) Blue light sensing cryptochromes: structure-function perspective and their genetic manipulation in plants. Proc Natl Acad Sci India 79:81–103
Kleine T, Lockhart P, Batschauer A (2003) An Arabidopsis protein closely related to Synechocystis cryptochrome is targeted to organelles. Plant J 35:93–103. https://doi.org/10.1046/j.1365-313X.2003.01787.x
Kleiner O, Kircher S, Harter K, Batschauer A (1999) Nuclear localization of the Arabidopsis blue light receptor cryptochrome 2. Plant J 19:289–296. https://doi.org/10.1046/j.1365-313x.1999.00535.x
Le Hir H, Nott A, Moore MJ (2003) How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28:215–220. https://doi.org/10.1016/S0968-0004(03)00052-5
Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Xing WD (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749. https://doi.org/10.1105/tpc.106.047688
Li YY, Mao K, Zhao C, Zhao XY, Zhang RF, Zhang HL, Shu HR, Hao YJ (2013) Molecular cloning and functional analysis of a blue light receptor gene MdCRY2 from apple (Malus domestica). Plant Cell Rep 32:555–566
Lin C (2002) Blue light receptors and signal transduction. Plant Cell 14:207–225. https://doi.org/10.1105/tpc.000646
Lin C, Shalitin D (2003) Cryptochrome structure and signal transduction. Annu Rev Plant Biol 54:469–496. https://doi.org/10.1146/annurev.arplant.54.110901.160901
Lin C, Ahmad M, Cashmore AR (1996) Arabidopsis cryptochrome 1 is a soluble protein mediating blue light-dependent regulation of plant growth and development. Plant J 10:893–902. https://doi.org/10.1046/j.1365-313X.1996.10050893.x
Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR (1998) Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc Natl Acad Sci USA 95:2686–2690. https://doi.org/10.1073/pnas.95.5.2686
Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han JH, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135:1481–1491. https://doi.org/10.1242/dev.020255
Liu Q, Wang Q, Deng W, Wang X, Piao M, Cai D, Li Y, Barshop WD, Yu X, Zhou T, Liu B, Oka Y, Wohlschlegel J, Zuo Z, Lin C (2017) Molecular basis for blue light-dependent phosphorylation of Arabidopsis cryptochrome 2. Nat Commun 8:1–12. https://doi.org/10.1038/ncomms15234
Lopez L, Carbone F, Bianco L, Giuliano G, Facella P, Perrotta G (2012) Tomato plants overexpressing cryptochrome 2 reveal altered expression of energy and stress-related gene products in response to diurnal cues. Plant Cell Environ 35:994–1012. https://doi.org/10.1111/j.1365-3040.2011.02467.x
Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277. https://doi.org/10.1038/360273a0
Mao J, Zhang YC, Sang Y, Li QH, Yang HQ (2005) A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci USA 102:12270–12275. https://doi.org/10.1073/pnas.0501011102
Marzi D, Brunetti P, Mele G, Napoli N, Calò L, Spaziani E, Matsui M, De Panfilis S, Costantino P, Serino G, Cardarelli M (2020) Light controls stamen elongation via cryptochromes, phytochromes and COP1 through HY5 and HYH. Plant J 103:379–394. https://doi.org/10.1111/tpj.14736
Mas P, Devlin PF, Panda S, Kay SA (2000) Functional interaction of phytochrome B and cryptochrome 2. Nature 408:207–211. https://doi.org/10.1038/35041583
Matsumura H, Kitajima H, Akada S, Abe J, Minaka N, Takahashi R (2009) Molecular cloning and linkage mapping of cryptochrome multigene family in soybean. Plant Genome 2:271–281. https://doi.org/10.3835/plantgenome.2009.06.0018
Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in arabidopsis leaf vascular development. Plant Physiol 131:1327–1339. https://doi.org/10.1104/pp.013623
Michaels SD, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky M, Amasino RM (2003) AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J 33:867–874. https://doi.org/10.1046/j.1365-313X.2003.01671.x
Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3:1–10. https://doi.org/10.1186/gb-2002-3-3-reviews0004
Mishra S, Khurana JP (2017) Emerging roles and new paradigms in signaling mechanisms of plant cryptochromes. CRC Crit Rev Plant Sci 36:89–115. https://doi.org/10.1080/07352689.2017.1348725
Mockler TC, Guo H, Yang H, Duong H, Lin C (1999) Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development 126:2073–2082. https://doi.org/10.1242/dev.126.10.2073
Mockler T, Yang H, Yu XH, Parikh D, Chia CY, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci USA 100:2140–2145. https://doi.org/10.1073/pnas.0437826100
Motchoulski A, Liscum E (1999) Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science 286:961–964. https://doi.org/10.1126/science.286.5441.961
Müller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18:586–597. https://doi.org/10.1105/tpc.105.038745
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004) Spiral1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding arabidopsis cells. Plant Cell 16:1178–1190. https://doi.org/10.1105/tpc.017830
Nakajima K, Kawamura T, Hashimoto T (2006) Role of the SPIRAL1 gene family in anisotropic growth of Arabidopsis thaliana. Plant Cell Physiol 47:513–522. https://doi.org/10.1093/pcp/pcj020
Ng M, Yanofsky MF (2001) Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13:739–753. https://doi.org/10.1105/tpc.13.4.739
Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466
Park HY, Lee SY, Seok HY, Kim SH, Sung ZR, Moon YH (2011) EMF1 interacts with EIP1, EIP6 or EIP9 involved in the regulation of flowering time in Arabidopsis. Plant Cell Physiol 52:1376–1388. https://doi.org/10.1093/pcp/pcr084
Payne CT, Zhang F, Lloyd AM (2000) GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1. Genetics 156:1349–1362. https://doi.org/10.1093/genetics/156.3.1349
Perrotta G, Ninu L, Flamma F, Weller JL, Kendrick RE, Nebuloso E, Giuliano G (2000) Tomato contains homologues of Arabidopsis cryptochromes 1 and 2. Plant Mol Biol 42:765–773. https://doi.org/10.1023/A:1006
Perrotta G, Yahoubyan G, Nebuloso E, Renzi L, Giuliano G (2001) Tomato and barley contain duplicated copies of cryptochrome 1. Plant Cell Environ 24:991–998. https://doi.org/10.1046/j.0016-8025.2001.00736.x
Platten JD, Foo E, Elliot RC, Hecht V, Reid JB, Weller JL (2005a) Cryptochrome 1 contributes to blue-light sensing in pea. Plant Physiol 139:1472–1482. https://doi.org/10.1104/pp.105.067462
Platten JD, Foo E, Foucher F, Hecht V, Reid JB, Weller JL (2005b) The cryptochrome gene family in pea includes two differentially expressed CRY2 genes. Plant Mol Biol 59:683–696. https://doi.org/10.1007/s11103-005-0828-z
Prakash S, Raut RN (1983) Artificial synthesis of Brassica napus and its prospects as an oilseed crop in India. Indian J Genet Plant Breed 43:282–290
Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93. https://doi.org/10.1038/nrm728
Rahman H, Bennett RA, Kebede B (2018) Molecular mapping of QTL alleles of Brassica oleracea affecting days to flowering and photosensitivity in spring Brassica napus. PLoS ONE 13:1–17. https://doi.org/10.1371/journal.pone.0189723
Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in arabidopsis and rice. Plant Physiol 134:1718–1732. https://doi.org/10.1104/pp.103.037788
Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435. https://doi.org/10.1093/pcp/pcf171
Sakai T, Wada T, Ishiguro S, Okada K (2000) RPT2: A signal transducer of the phototropic response in Arabidopsis. Plant Cell 12:225–236. https://doi.org/10.1105/tpc.12.2.225
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of constans target genes in reproductive development of Arabidopsis. Science 288:1613–1616. https://doi.org/10.1126/science.288.5471.1613
Santos MA (1991) An improved method for the small scale preparation of bacteriophage DNA based on phage precipitation by zinc chloride. Nucleic Acids Res 19:5442. https://doi.org/10.1093/nar/19.19.5442
Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, Chory J (1999) The Arabidopsis det3 mutant reveals a central role for the vacuolar H+- ATPase in plant growth and development. Genes Dev 13:3259–3270. https://doi.org/10.1101/gad.13.24.3259
Shalitin D, Yang H, Mockler TC, Maymon M, Guo H, Whitelam GC, Lin C (2002) Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417:763–767. https://doi.org/10.1038/natur
Sharma P, Chatterjee M, Burman N, Khurana JP (2014) Cryptochrome 1 regulates growth and development in Brassica through alteration in the expression of genes involved in light, phytohormone and stress signalling. Plant Cell Environ 37:961–977. https://doi.org/10.1111/pce.12212
Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koornneef M, Ausubel FM, Goodman HM (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 8:659–671. https://doi.org/10.1046/j.1365-313X.1995.08050659.x
Shoji T, Narita NN, Hayashi K, Asada J, Hamada T, Sonobe S, Nakajima K, Hashimoto T (2004) Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol 136:3933–3944. https://doi.org/10.1104/pp.104.051748
Small GD, Min B, Lefebvre PA (1995) Characterization of a Chlamydomonas reinhardtii gene encoding a protein of the DNA photolyase/blue light photoreceptor family. Plant Mol Biol 28:443–454
Somers DE, Devlin PF, Kay SA (1998) Phytochromes and Cryptochromes in the Entrainment of the Arabidopsis Circadian Clock Published by : American Association for the Advancement of Science Stable
Song SK, Clark SE (2005) POL and related phosphatases are dosage-sensitive regulators of meristem and organ development in Arabidopsis. Dev Biol 285:272–284. https://doi.org/10.1016/j.ydbio.2005.06.020
Song SK, Lee MM, Clark SE (2006) POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells. Development 133:4691–4698. https://doi.org/10.1242/dev.02652
Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120
Thakur JK, Tyagi AK, Khurana JP (2001) OsIAA1, an Aux/IAA cDNA from rice, and changes in its expression as influenced by auxin and light. DNA Res 8:193–203. https://doi.org/10.1093/dnares/8.5.193
Thakur JK, Malik MR, Bhatt V, Reddy MK, Sopory SK, Tyagi AK, Khurana JP (2003) A POLYCOMB group gene of rice (Oryza sativa L. subspecies indica), OsiEZ1, codes for a nuclear-localized protein expressed preferentially in young seedlings and during reproductive development. Gene 314:1–13. https://doi.org/10.1016/S0378-1119(03)00723-6
Varagona MJ, Schmidt RJ, Raikhel NV (1992) Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein opaque-2. Plant Cell 4:1213–1227. https://doi.org/10.1105/tpc.4.10.1213
Vigneault F, Lachance D, Cloutier M, Pelletier G, Levasseur C, Séguin A (2007) Members of the plant NIMA-related kinases are involved in organ development and vascularization in poplar, Arabidopsis and rice. Plant J 51:575–588. https://doi.org/10.1111/j.1365-313X.2007.03161.x
Wang Q, Zuo Z, Wang X, Gu L, Yoshizumi T, Yang Z, Yang L, Liu Q, Liu W, Han YJ, Kim J, Liu L, Wohlschlegel J, Matsui M, Oka Y, Lin C (2016) Photoactivation and inactivation of Arabidopsis cryptochrome 2. Science 354:343–347. https://doi.org/10.4049/jimmunol.1801473
Wang F, Robson TM, Casal JJ, Shapiguzov A, Aphalo PJ (2020) Contributions of cryptochromes and phototropins to stomatal opening through the day. Funct Plant Biol 47:226–238. https://doi.org/10.1071/FP19053
Wen J, Lease KA, Walker JC (2004) DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J 37:668–677. https://doi.org/10.1111/j.1365-313X.2003.01994.x
Wray GA (2003) Transcriptional regulation and the evolution of development. Int J Dev Biol 47:675–684. https://doi.org/10.1387/ijdb.14756343
Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20:1377–1419. https://doi.org/10.1093/molbev/msg140
Xie XZ, Chen ZP, Wang XJ (2005) Cloning and expression analysis of CRY2 gene in Sorghum bicolor. Journal of Plant Physiol and Mol Biol 31(3):261–268
Xu P, Xiang Y, Zhu H, Xu H, Zhang Z, Zhang C, Zhang L, Ma Z (2009) Wheat cryptochromes: subcellular localization and involvement in photomorphogenesis and osmotic stress responses. Plant Physiol 149:760–774. https://doi.org/10.1104/pp.108.132217
Xu P, Zhu HL, Bin XuH, Zhang ZZ, Zhang CQ, Zhang LX, Ma ZQ (2010) Composition and phylogenetic analysis of wheat cryptochrome gene family. Mol Biol Rep 37:825–832. https://doi.org/10.1007/s11033-009-9628-x
Yamamoto YY, Matsui M, Ang LH, Deng XW (1998) Role of a COP1 interactive protein in mediating light-regulated gene expression in arabidopsis. Plant Cell 10:1083–1094. https://doi.org/10.1105/tpc.10.7.1083
Yang G, Komatsu S (2004) Molecular cloning and characterization of a novel brassinolide enhanced gene OsBLE1 in Oryza sativa seedlings. Plant Physiol Biochem 42:1–6. https://doi.org/10.1016/j.plaphy.2003.10.001
Yang L, Fu J, Qi S, Hong Y, Huang H, Dai S (2017) Molecular cloning and function analysis of ClCRY1a and ClCRY1b, two genes in Chrysanthemum lavandulifolium that play vital roles in promoting floral transition. Gene 617:32–43. https://doi.org/10.1016/j.gene.2017.02.020
Yu LP, Simon EJ, Trotochaud AE, Clark SE (2000) POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci. Development 127:1661–1670. https://doi.org/10.1242/dev.127.8.1661
Yu H, Xu Y, Tan EL, Kumar PP (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. PNAS 99:16336–16341
Yu LP, Miller AK, Clark SE (2003) POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Curr Biol 13:179–188. https://doi.org/10.1016/S0960-9822(03)00042-3
Yu X, Klejnot J, Zhao X, Shalitin D, Maymon M, Yang H, Lee J, Liu X, Lopez J, Lina C (2007) Arabidopsis cryptochrome 2 completes its posttranslational life cycle in the nucleus. Plant Cell 19:3146–3156. https://doi.org/10.1105/tpc.107.053017
Yu X, Liu H, Klejnot J, Lin C (2010) The cryptochrome blue light receptors. Arab B 8:e0135. https://doi.org/10.1016/j.earlhumdev.2006.05.022
Zhang YC, Gong SF, Li QH, Sang Y, Yang HQ (2006) Functional and signaling mechanism analysis of rice CRYPTOCHROME 1. Plant J 46:971–983. https://doi.org/10.1111/j.1365-313X.2006.02753.x
Zhang Q, Li H, Li R, Hu R, Fan C, Chen F, Wang Z, Liu X, Fu Y, Lin C (2008) Association of the circadian rhythmic expression of GmCRY1a with a latitudinal cline in photoperiodic flowering of soybean. Proc Natl Acad Sci USA 105:21028–21033. https://doi.org/10.1073/pnas.0810585105
Zhao QP, Zhu JD, Li NN, Wang XN, Zhao X, Zhang X (2020) Cryptochrome-mediated hypocotyl phototropism was regulated antagonistically by gibberellic acid and sucrose in Arabidopsis. J Integr Plant Biol 62:614–630. https://doi.org/10.1111/jipb.12813
Acknowledgements
This research was funded by the Department of Biotechnology, Government of India (Grant No. BT/AGIII/CARI/01/2012) and the J.C. Bose National Fellowship to JPK by the Science and Engineering Research Board (SERB), Government of India. Authors also acknowledge the infrastructural support provided by the Department of Science and Technology (FIST and PURSE programmes), Government of India, and the University Grants Commission (UGC-SAP), New Delhi. The award of Senior Research Fellowship from the Council of Scientific and Industrial Research, New Delhi, to PS, SM, NB, NB, SS and MC is duly acknowledged. is duly acknowledged. Authors are grateful to Dr. T. Mohapatra (ICAR, New Delhi) for his support from time to time during the course of this investigation.
Funding
This research was funded by the Department of Biotechnology, Government of India (Grant No. BT/AGIII/CARI/01/2012) and the J.C. Bose National Fellowship to JPK by the Science and Engineering Research Board (SERB), Government of India.
Author information
Authors and Affiliations
Contributions
JPK and PS planned and designed the research; PS, SM, NB and MC performed experiments and analyzed the data. PS wrote the manuscript with contributions from SM, NB, MC and SS. AKP provided useful suggestions during the course of study. All authors contributed in writing and editing of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
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.
Rights and permissions
About this article
Cite this article
Sharma, P., Mishra, S., Burman, N. et al. Characterization of Cry2 genes (CRY2a and CRY2b) of B. napus and comparative analysis of BnCRY1 and BnCRY2a in regulating seedling photomorphogenesis. Plant Mol Biol 110, 161–186 (2022). https://doi.org/10.1007/s11103-022-01293-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-022-01293-6