Identification and characterisation of blue light photoreceptor gene family and their expression in tomato (Solanum lycopersicum) under cold stress
Agossa Anicet Batcho
A B * , Joy Oluchi Nwogwugwu C , Mohsin Ali D , Basit Jabbar E , Ayesha Javaid F and Martin Fellner B
+ Author Affiliations
- Author Affiliations
A National University of Sciences, Technology, Engineering and Mathematics (ENS-UNSTIM), Natitingou, Republic of Benin.
B Laboratory of Growth Regulators, Institute of Experimental Botany of the Czech Academy of Sciences, Palacký University, Šlechtitelů 27, Olomouc-Holice 783 71, Czech Republic.
C Department of Forest Conservation and Protection, Forestry Research Institute of Nigeria, Ibadan, Nigeria.
D Independent Researcher, House No. 280 A/1 Sector F1 Mirpur 10250, AJK, Pakistan.
E Centre of Excellence in Molecular Biology, University of the Punjab Lahore, Pakistan.
F Independent Researcher, Askari 13, Rawalpandi 46604, Pakistan.
Functional Plant Biology 49(7) 647-658 https://doi.org/10.1071/FP21297
Submitted: 17 February 2021 Accepted: 7 March 2022 Published: 19 April 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The Arabidopsis thaliana L. photoreceptor genes homologues in tomato (Solanum lycopersicum L.) genome were analysed using bioinformatic tools. The expression pattern of these genes under cold stress was also evaluated. Transcriptome analysis of the tomato sequence revealed that the photoreceptor gene family is involved in abiotic stress tolerance. They participate in various pathways and controlling multiple metabolic processes. They are structurally related to PAS, LIGHT-OXYGEN-VOLTAGE-SENSING (LOV), DNA photolyase, 5,10-methenyl tetrahydrofolate (MTHF), flavin-binding kelch F-box, GAF, PHY, Seven-bladed β-propeller and C27 domains. They also interact with flavin adenine dinucleotide (FAD), (5S)-5-methyl-2-(methylsulfanyl)-5-phenyl-3-(phenylamino)-3,5-dihydro-4H-imidazol-4-one (FNM) and Phytochromobilin (PϕB) ligands. These interactions help to create a cascade of protein phosphorylation involving in cell defence transcription or stress-regulated genes. They localisation of these gene families on tomato chromosomes appeared to be uneven. Phylogenetic tree of tomato and Arabidopsis photoreceptor gene family were classified into eight subgroups, indicating gene expression diversity. Morphological and physiological assessment revealed no dead plant after 4 h of cold treatment. All the plants were found to be alive, but there were some variations in the data across different parameters. Cold stress significantly reduced the rate of photosynthesis from 10.06 to 3.16 μmol m−2 s−1, transpiration from 4.6 to 1.3 mmol m−2 s−1, and stomatal conductance from 94.6 to 25.6 mmol m−2 s−1. The cold stressed plants also had reduced height, root/shoot length, and fresh/dry biomass weight than the control plants. Relative expression analysis under cold stress revealed that after 4 h, light stimulates the transcript level of Cry2 from 1.9 to 5.7 and PhyB from 0.98 to 6.9 compared to other photoreceptor genes.
Keywords: abiotic stress tolerance, bioinformatics, blue light signaling, expression analysis, photoreceptor genes, photosynthesis, tomato, transcriptome data.
References
Ahmad M (2016) Photocycle and signaling mechanisms of plant cryptochromes. Current Opinion in Plant Biology 33, 108–115.| Photocycle and signaling mechanisms of plant cryptochromes.Crossref | GoogleScholarGoogle Scholar | 27423124PubMed |
Allwood JW, Williams A, Uthe H, van Dam NM, Mur LAJ, Grant MR, Pétriacq P (2021) Unravelling plant responses to stress—the importance of targeted and untargeted metabolomics. Metabolites 11, 558
| Unravelling plant responses to stress—the importance of targeted and untargeted metabolomics.Crossref | GoogleScholarGoogle Scholar | 34436499PubMed |
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
| Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar | 9254694PubMed |
Ballaré CL (2009) Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. Plant, Cell & Environment 32, 713–725.
| Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence.Crossref | GoogleScholarGoogle Scholar |
Batcho AA, Sarwar MB, Tariq L, Rashid B, Hassan S, Husnain T (2020) Identification and characterisation of heat shock protein gene (HSP70) family and its expression in Agave sisalana under heat stress. The Journal of Horticultural Science and Biotechnology 95, 470–482.
| Identification and characterisation of heat shock protein gene (HSP70) family and its expression in Agave sisalana under heat stress.Crossref | GoogleScholarGoogle Scholar |
Carvalho RF, Campos ML, Azevedo RA (2013) The role of phytochromes in stress tolerance. In ‘Salt stress in plants’. (Eds P Ahmad, MM Azooz, MNV Prasad) (Springer: New York, NY)
| Crossref |
Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen L-O, van der Horst GTJ, Batschauer A, Ahmad M (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annual Review of Plant Biology 62, 335–364.
| The cryptochromes: blue light photoreceptors in plants and animals.Crossref | GoogleScholarGoogle Scholar | 21526969PubMed |
Christie JM, Blackwood L, Petersen J, Sullivan S (2015) Plant flavoprotein photoreceptors. Plant and Cell Physiology 56, 401–413.
Consentino L, Lambert S, Martino C, Jourdan N, Bouchet PE, Witczak J, d’Harlingue A (2015) Blue-light dependent reactive oxygen species formation by Arabidopsis cryptochrome may define a novel evolutionarily conserved signaling mechanism. New Phytologist 206, 1450–1462.
| Blue-light dependent reactive oxygen species formation by Arabidopsis cryptochrome may define a novel evolutionarily conserved signaling mechanism.Crossref | GoogleScholarGoogle Scholar |
D’Amico-Damião V, Carvalho RF (2018) Cryptochrome-related abiotic stress responses in plants. Frontiers in Plant Science 9, 1897
| Cryptochrome-related abiotic stress responses in plants.Crossref | GoogleScholarGoogle Scholar | 30619439PubMed |
D’Amico-Damião V, Cruz FJR, Gavassi MA, Santos DMM, Melo HC, Carvalho RF (2015) Photomorphogenic modulation of water stress in tomato (Solanum lycopersicum L.): the role of phytochromes A, B1, and B2. The Journal of Horticultural Science and Biotechnology 90, 25–30.
| Photomorphogenic modulation of water stress in tomato (Solanum lycopersicum L.): the role of phytochromes A, B1, and B2.Crossref | GoogleScholarGoogle Scholar |
Dar AA, Choudhury AR, Kancharla PK, Arumugam N (2017) The FAD2 gene in plants: occurrence, regulation, and role. Frontiers in Plant Science 8, 1789
| The FAD2 gene in plants: occurrence, regulation, and role.Crossref | GoogleScholarGoogle Scholar | 29093726PubMed |
Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytologist 221, 32–49.
| Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration.Crossref | GoogleScholarGoogle Scholar |
El-Esawi M, Arthaut L-D, Jourdan N, d’Harlingue A, Link J, Martino CF, Ahmad M (2017) Blue-light induced biosynthesis of ROS contributes to the signaling mechanism of Arabidopsis cryptochrome. Scientific Reports 7, 13875
| Blue-light induced biosynthesis of ROS contributes to the signaling mechanism of Arabidopsis cryptochrome.Crossref | GoogleScholarGoogle Scholar | 29066723PubMed |
Elbadrawy E, Sello A (2016) Evaluation of nutritional value and antioxidant activity of tomato peel extracts. Arabian Journal of Chemistry 9, S1010–S1018.
| Evaluation of nutritional value and antioxidant activity of tomato peel extracts.Crossref | GoogleScholarGoogle Scholar |
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. Plant Physiology 179, 732–748.
| Pivotal roles of cryptochromes 1a and 2 in tomato development and physiology.Crossref | GoogleScholarGoogle Scholar | 30541876PubMed |
Fraser GE, Jacobsen BK, Knutsen SF, Mashchak A, Loren JI (2020) Tomato consumption and intake of lycopene as predictors of the incidence of prostate cancer: the Adventist Health Study-2. Cancer Causes & Control 31, 341–351.
| Tomato consumption and intake of lycopene as predictors of the incidence of prostate cancer: the Adventist Health Study-2.Crossref | GoogleScholarGoogle Scholar |
Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Molecular Plant 9, 1353–1365.
| The multifaceted roles of HY5 in plant growth and development.Crossref | GoogleScholarGoogle Scholar | 27435853PubMed |
Gavassi MA, Monteiro CC, Campos ML, Melo HC, Carvalho RF (2017) Phytochromes are key regulators of abiotic stress responses in tomato. Scientia Horticulturae 222, 126–135.
| Phytochromes are key regulators of abiotic stress responses in tomato.Crossref | GoogleScholarGoogle Scholar |
Gil K-E, Park C-M (2019) Thermal adaptation and plasticity of the plant circadian clock. New Phytologist 221, 1215–1229.
| Thermal adaptation and plasticity of the plant circadian clock.Crossref | GoogleScholarGoogle Scholar |
Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Molecular Biology 17, 1233–1240.
| Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1834244PubMed |
Guy CL (2003) Freezing tolerance of plants: current understanding and selected emerging concepts. Canadian Journal of Botany 81, 1216–1223.
| Freezing tolerance of plants: current understanding and selected emerging concepts.Crossref | GoogleScholarGoogle Scholar |
Henry JT, Crosson S (2011) Ligand-binding PAS domains in a genomic, cellular, and structural context. Annual Review of Microbiology 65, 261–286.
| Ligand-binding PAS domains in a genomic, cellular, and structural context.Crossref | GoogleScholarGoogle Scholar | 21663441PubMed |
Hernández ML, Padilla MN, Sicardo MD, Mancha M, Martínez-Rivas JM (2011) Effect of different environmental stresses on the expression of oleate desaturase genes and fatty acid composition in olive fruit. Phytochemistry 72, 178–187.
| Effect of different environmental stresses on the expression of oleate desaturase genes and fatty acid composition in olive fruit.Crossref | GoogleScholarGoogle Scholar | 21194717PubMed |
Hernández ML, Sicardo MD, Alfonso M, Martínez-Rivas JM (2019) Transcriptional regulation of stearoyl-acyl carrier protein desaturase genes in response to abiotic stresses leads to changes in the unsaturated fatty acids composition of olive mesocarp. Frontiers in Plant Science 10, 251
| Transcriptional regulation of stearoyl-acyl carrier protein desaturase genes in response to abiotic stresses leads to changes in the unsaturated fatty acids composition of olive mesocarp.Crossref | GoogleScholarGoogle Scholar | 30891055PubMed |
Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nature Reviews Genetics 8, 217–230.
| Light-regulated transcriptional networks in higher plants.Crossref | GoogleScholarGoogle Scholar | 17304247PubMed |
Jourdan N, Martino CF, El-Esawi M, Witczak J, Bouchet P-E, d’Harlingue A, Ahmad M (2015) Blue-light dependent ROS formation by Arabidopsis cryptochrome-2 may contribute toward its signaling role. Plant Signaling & Behavior 10, e1042647
| Blue-light dependent ROS formation by Arabidopsis cryptochrome-2 may contribute toward its signaling role.Crossref | GoogleScholarGoogle Scholar |
Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354, 886–889.
| Phytochromes function as thermosensors in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27789797PubMed |
Khazanov NA, Carlson HA (2013) Exploring the composition of protein-ligand binding sites on a large scale. PLoS Computational Biology 9, e1003321
| Exploring the composition of protein-ligand binding sites on a large scale.Crossref | GoogleScholarGoogle Scholar | 24277997PubMed |
Kim H-J, Kim Y-K, Park J-Y, Kim J (2002) Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. The Plant Journal 29, 693–704.
| Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12148528PubMed |
Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annual Review of Genetics 39, 309–338.
| Orthologs, paralogs, and evolutionary genomics.Crossref | GoogleScholarGoogle Scholar | 16285863PubMed |
Kurepin LV, Dahal KP, Savitch LV, Singh J, Bode R, Ivanov AG, Hurry V, Hüner NPA (2013) Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation. International Journal of Molecular Sciences 14, 12729–12763.
| Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation.Crossref | GoogleScholarGoogle Scholar | 23778089PubMed |
Legris M, Klose C, Burgie ES, Rojas CR, Neme M, Hiltbrunner A, Casal JJ (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897–900.
| Phytochrome B integrates light and temperature signals in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27789798PubMed |
Li N, Euring D, Cha JY, Lin Z, Lu M, Huang L-J, Kim WY (2021) Plant hormone-mediated regulation of heat tolerance in response to global climate change. Frontiers in Plant Science 11, 627969
| Plant hormone-mediated regulation of heat tolerance in response to global climate change.Crossref | GoogleScholarGoogle Scholar | 33643337PubMed |
Lichtarge O, Bourne HR, Cohen FE (1996) An evolutionary trace method defines binding surfaces common to protein families. Journal of Molecular Biology 257, 342–358.
| An evolutionary trace method defines binding surfaces common to protein families.Crossref | GoogleScholarGoogle Scholar | 8609628PubMed |
Mao J, Zhang Y-C, Sang Y, Li Q-H, Yang H-Q (2005) A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proceedings of the National Academy of Sciences of the United States of America 102, 12270–12275.
| A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening.Crossref | GoogleScholarGoogle Scholar | 16093319PubMed |
Mawkhiew HB, Sahoo L, Kharshiing EV (2021) Gene-to-trait knowledge graphs show association of plant photoreceptors with physiological and developmental processes that can confer agronomic benefits. Genetic Resources and Crop Evolution 68, 2727–2735.
| Gene-to-trait knowledge graphs show association of plant photoreceptors with physiological and developmental processes that can confer agronomic benefits.Crossref | GoogleScholarGoogle Scholar |
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33, 453–467.
| Reactive oxygen species homeostasis and signalling during drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar |
Molas ML, Kiss JZ (2009) Phototropism and gravitropism in plants. Advances in Botanical Research 49, 1–34.
Oliveira G, Peñuelas J (2005) Effects of winter cold stress on photosynthesis and photochemical efficiency of PSII of the Mediterranean Cistus albidus L. and Quercus ilex L. Plant Ecology 175, 179–191.
| Effects of winter cold stress on photosynthesis and photochemical efficiency of PSII of the Mediterranean Cistus albidus L. and Quercus ilex L.Crossref | GoogleScholarGoogle Scholar |
Ostmeyer T, Parker N, Jaenisch B, Alkotami L, Bustamante C, Jagadish SVK (2020) Impacts of heat, drought, and their interaction with nutrients on physiology, grain yield, and quality in field crops. Plant Physiology Reports 25, 549–568.
| Impacts of heat, drought, and their interaction with nutrients on physiology, grain yield, and quality in field crops.Crossref | GoogleScholarGoogle Scholar |
Panchy N, Lehti-Shiu M, Shiu S-H (2016) Evolution of gene duplication in plants. Plant Physiology 171, 2294–2316.
| Evolution of gene duplication in plants.Crossref | GoogleScholarGoogle Scholar | 27288366PubMed |
Phee B-K, Park S, Cho J-H, Jeon J-S, Bhoo SH, Hahn T-R (2007) Comparative proteomic analysis of blue light signaling components in the Arabidopsis cryptochrome 1 mutant. Molecules & Cells 23, 154–160.
Pooam M, Dixon N, Hilvert M, Misko P, Waters K, Jourdan N, Ahmad M (2021) Effect of temperature on the Arabidopsis cryptochrome photocycle. Physiologia Plantarum 172, 1653–1661.
| Effect of temperature on the Arabidopsis cryptochrome photocycle.Crossref | GoogleScholarGoogle Scholar | 33583025PubMed |
Puggioni MP (2020) Dynamic regulation of oxygenic photosynthesis: study of long term acclimation to photo-oxidative stress induced by excess of light. Dissertation, Heinrich Heine University Düsseldorf.
Rodziewicz P, Swarcewicz B, Chmielewska K, Wojakowska A, Stobiecki M (2014) Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiologiae Plantarum 36, 1–19.
| Influence of abiotic stresses on plant proteome and metabolome changes.Crossref | GoogleScholarGoogle Scholar |
Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40, 13–29.
| Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships.Crossref | GoogleScholarGoogle Scholar |
Sancar A (2003) Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chemical Reviews 103, 2203–2238.
| Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors.Crossref | GoogleScholarGoogle Scholar | 12797829PubMed |
Saradadevi R, Palta JA, Siddique KHM (2017) ABA-mediated stomatal response in regulating water use during the development of terminal drought in wheat. Frontiers in Plant Science 8, 1251
| ABA-mediated stomatal response in regulating water use during the development of terminal drought in wheat.Crossref | GoogleScholarGoogle Scholar | 28769957PubMed |
Shah KK, Modi B, Lamsal B, Shrestha J, Aryal SP (2021) Bioactive compounds in tomato and their roles in disease prevention. Fundamental and Applied Agriculture (FAA) 6, 210–224.
Shahryar N, Maali-Amiri R (2016) Metabolic acclimation of tetraploid and hexaploid wheats by cold stress-induced carbohydrate accumulation. Journal of Plant Physiology 204, 44–53.
| Metabolic acclimation of tetraploid and hexaploid wheats by cold stress-induced carbohydrate accumulation.Crossref | GoogleScholarGoogle Scholar | 27500556PubMed |
Solanke AU, Sharma AK (2008) Signal transduction during cold stress in plants. Physiology and Molecular Biology of Plants 14, 69–79.
| Signal transduction during cold stress in plants.Crossref | GoogleScholarGoogle Scholar | 23572874PubMed |
Su J, Liu B, Liao J, Yang Z, Lin C, Oka Y (2017) Coordination of cryptochrome and phytochrome signals in the regulation of plant light responses. Agronomy 7, 25
| Coordination of cryptochrome and phytochrome signals in the regulation of plant light responses.Crossref | GoogleScholarGoogle Scholar |
Suzuki N, Katano K (2018) Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack. Frontiers in Plant Science 9, 490
| Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack.Crossref | GoogleScholarGoogle Scholar | 29713332PubMed |
Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology 28, 463–487.
| Hormonal interactions in the regulation of plant development.Crossref | GoogleScholarGoogle Scholar | 22856461PubMed |
Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Frontiers in Plant Science 8, 161
| Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects.Crossref | GoogleScholarGoogle Scholar | 28265276PubMed |
Wang X, Cai X, Xu C, Wang Q, Dai S (2016) Drought-responsive mechanisms in plant leaves revealed by proteomics. International Journal of Molecular Sciences 17, 1706
| Drought-responsive mechanisms in plant leaves revealed by proteomics.Crossref | GoogleScholarGoogle Scholar |
Wang Z, Li G, Sun H, Ma L, Guo Y, Zhao Z, Gao H, Mei L (2018) Effects of drought stress on photosynthesis and photosynthetic electron transport chain in young apple tree leaves. Biology Open 7, bio035279
| Effects of drought stress on photosynthesis and photosynthetic electron transport chain in young apple tree leaves.Crossref | GoogleScholarGoogle Scholar | 30127094PubMed |
Wang T, Dong Q, Wang W, Chen S, Cheng Y, Tian H, Li X, Hussain S, Wang L, Gong L, Wang S (2021) Evolution of AITR family genes in cotton and their functions in abiotic stress tolerance. Plant Biology 23, 58–68.
| Evolution of AITR family genes in cotton and their functions in abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 33202099PubMed |
Wei J, Zheng G, Dong X, Li H, Liu S, Wang Y, Liu Z (2022) Integration of transcriptome and proteome analysis reveals the mechanism of freezing tolerance in winter rapeseed. Plant Growth Regulation 96, 103–118.
| Integration of transcriptome and proteome analysis reveals the mechanism of freezing tolerance in winter rapeseed.Crossref | GoogleScholarGoogle Scholar |
Yadav SK (2010) Cold stress tolerance mechanisms in plants. A review. Agronomy for Sustainable Development 30, 515–527.
| Cold stress tolerance mechanisms in plants. A review.Crossref | GoogleScholarGoogle Scholar |
Zhu W, Lyu F, Naumovski N, Ajlouni S, Ranadheera CS (2020) Functional efficacy of probiotic lactobacillus sanfranciscensis in apple, orange and tomato juices with special reference to storage stability and in vitro gastrointestinal survival. Beverages 6, 13
| Functional efficacy of probiotic lactobacillus sanfranciscensis in apple, orange and tomato juices with special reference to storage stability and in vitro gastrointestinal survival.Crossref | GoogleScholarGoogle Scholar |
