Unraveling barley's PAL gene family: a genome-wide study on defense mechanisms against Puccinia graminis f. sp. tritici

Authors

  • Thamer ALBALAWI Prince Sattam Bin Abdulaziz University, College of Science and Humanities, Department of Biology, Alkharj 11942 (SA)

DOI:

https://doi.org/10.15835/nbha52313854

Keywords:

H. vulgare , Puccinia graminis f. sp. Tritici, Phenylalanine ammonia-lyase (PAL), Barley, Transcriptomic, Gene regulation

Abstract

Phenylalanine ammonia lyase (PAL) is a pivotal enzyme bridging primary and secondary phenylpropanoid metabolism, influencing plant growth, development, and stress responses. Despite extensive studies on PAL genes across various plant species, their investigation in barley, a critical staple food globally, has been relatively scarce. In this study, we have successfully identified 10 HvPAL genes, designated as HvPAL genes, in Hordeum vulgare (barley). These HvPAL genes were categorized based on their conserved sequences, which revealed patterns through MEME analysis and multiple sequence alignment. Interestingly, we found cis elements related to stress in the promoter regions of HvPAL genes, indicating their involvement in the response to pathogens. Furthermore, these gene promoters contained components associated with light, development, and hormone responsiveness. This suggests that they may play a role in hormonal developmental processes. MicroRNAs were also identified as regulators of the HvPAL genes we identified highlighting their significance in barley. To further investigate these gene expression patterns, we analyzed the RNA-seq data revealed the upregulating of HvPAL 2, HvPAL3, and HvPAL8, and downregulating HvPAL 5, HvPAL 6, and HvPAL9 genes in this study. This study focused on the regulation of PAL genes in response to 23 different races of Puccinia graminis f. sp. tritici in barley. These results suggest ways to improve traits and develop barley varieties that are resistant to pathogens by selectively increasing the expression of certain HvPAL genes that were not previously regulated. This thorough investigation aims to expand our knowledge of the versatility of the PAL gene family, providing insights for advancements in host -pathogen genetics.

References

Abdulla MF, Mostafa K, Aydin A, Kavas M, Aksoy E (2024). GATA transcription factor in common bean: A comprehensive genome-wide functional characterization, identification, and abiotic stress response evaluation. Plant Molecular Biology 114(3):43. https://doi.org/10.1007/s11103-024-01443-y

Adams KL, Wendel JF (2005). Polyploidy and genome evolution in plants. Current Opinion in Plant Biology 8(2):135-41. https://doi.org/10.1016/j.pbi.2005.01.001

Ain-Ali QU, Mushtaq N, Amir R, Gul A, Tahir M, Munir F (2021). Genome-wide promoter analysis, homology modeling and protein interaction network of Dehydration Responsive Element Binding (DREB) gene family in Solanum tuberosum. PLoS One 16(12):e0261215. https://doi.org/10.1371/journal.pone.0261215

Barre A, Culerrier R, Granier C, Selman L, Peumans WJ, Van Damme EJ, Bienvenu F, Bienvenu J, Rougé P (2009). Mapping of IgE-binding epitopes on the major latex allergen Hev b 2 and the cross-reacting 1,3 beta-glucanase fruit allergens as a molecular basis for the latex-fruit syndrome. Molecular Immunology 46(8-9):1595-1604. https://doi.org/10.1016/j.molimm.2008.12.007

Bartwal A, Mall R, Lohani P, Guru SK, Arora S (2013). Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. Journal of Plant Growth Regulation 32:216-232. http://dx.doi.org/10.1007/s00344-012-9272-x

Bülow L, Hehl R (2016). Bioinformatic identification of conserved cis-sequences in coregulated genes. Plant Synthetic Promoters. Methods in Molecular Biology 1482: 233-245. https://doi.org/10.1007/978-1-4939-6396-6_15

Calero P, Nikel PI (2019). Chasing bacterial chassis for metabolic engineering: a perspective review from classical to non-traditional microorganisms. Microbial Biotechnology 12(1):98-124. https://doi.org/10.1111/1751-7915.13292

Cass CL, Peraldi A, Dowd PF, Mottiar Y, Santoro N, Karlen SD, … Sedbrook JC (2015). Effects of phenylalanine ammonia lyase (PAL) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium. Journal of Experimental Botany 66(14):4317-35. https://doi.org/10.1093/jxb/erv269

Chen Y, Fang T, Su H, Duan S, Ma R, Wang P, … Dong X (2023). A reference-grade genome assembly for Astragalus mongholicus and insights into the biosynthesis and high accumulation of triterpenoids and flavonoids in its roots. Plant Communications 4(2):100469. https://doi.org/10.1016/j.xplc.2022.100469

Chen Y, Li F, Tian L, Huang M, Deng R, Li X, … Wu G (2017). The phenylalanine ammonia lyase gene LjPAL1 is involved in plant defense responses to pathogens and plays diverse roles in Lotus japonicus-rhizobium symbioses. Molecular Plant Microbe Interaction 30(9):739-753. https://doi.org/10.1094/mpmi-04-17-0080-r

De Schutter K, Van Damme EJ (2015). Protein-carbohydrate interactions as part of plant defense and animal immunity. Molecules 20(5):9029-9053. https://doi.org/10.3390%2Fmolecules20059029

Dehghan S, Sadeghi M, Pöppel A, Fischer R, Lakes-Harlan R, Kavousi HR, Vilcinskas A, Rahnamaeian M (2014). Differential inductions of phenylalanine ammonia-lyase and chalcone synthase during wounding, salicylic acid treatment, and salinity stress in safflower, Carthamus tinctorius. Bioscience Reports 34(3):e00114. https://doi.org/10.1042%2FBSR20140026

Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L (2002). The phenylpropanoid pathway and plant defence—a genomics perspective. Molecular Plant Pathology 3(5):371-390. https://doi.org/10.1046/j.1364-3703.2002.00131.x

Djami-Tchatchou AT, Sanan-Mishra N, Ntushelo K, Dubery IA (2017). Functional roles of microRNAs in agronomically important plants-potential as targets for crop improvement and protection. Frontiers in Plant Science 8:378. https://doi.org/10.3389/fpls.2017.00378

Dong CJ, Shang QM (2013). Genome-wide characterization of phenylalanine ammonia-lyase gene family in watermelon (Citrullus lanatus). Planta 238:35-49. https://doi.org/10.1007/s00425-013-1869-1

Forster B, Ellis RP, Thomas WTB, Newton AC, Tuberosa R, This D, El-Enein RA, Bahri MH, Salem MB (2000). The development and application of molecular markers for abiotic stress tolerance in barley. Journal of Experimental Botany 51(342):19-27. https://doi.org/10.1093/jexbot/51.342.19

Grando S, Macpherson HG (2005). Food barley: importance, uses and local knowledge. ICARDA, Aleppo, Syria, pp 121-137. https://repo.mel.cgiar.org/handle/20.500.11766/67677

Guo J, Wang MH (2009). Characterization of the phenylalanine ammonia-lyase gene (SlPAL5) from tomato (Solanum lycopersicum L.). Molecular Biology Reports 36:1579-1585. https://doi.org/10.1007/s11033-008-9354-9

Guo ZH, Ma PF, Yang GQ, Hu JY, Liu YL, Xia EH, … Li DZ (2019). Genome sequences provide insights into the reticulate origin and unique traits of woody bamboos. Molecular Plant 12(10):1353-1365. https://doi.org/10.1016/j.molp.2019.05.009

Haberle V, Lenhard B (2016). Promoter architectures and developmental gene regulation. Seminars in Cell & Developmental Biology 57:11-23. https://doi.org/10.1016/j.semcdb.2016.01.014

Hahlbrock K, Scheel D (1989). Physiology and molecular biology of phenylpropanoid metabolism. Annual Review of Plant Biology 40(1):347-369. https://10.1146/annurev.pp.40.060189.002023

Haider MZ, Sami A, Shafiq M, Anwar W, Ali S, Ali Q, … Alarifi S (2023). Genome-wide identification and in-silico expression analysis of carotenoid cleavage oxygenases gene family in Oryza sativa (rice) in response to abiotic stress. Frontiers in Plant Science 4:1269995. https://doi.org/10.3389%2Ffpls.2023.1269995

Irfan U, Haider M, Shafiq M, Sami A, Ali Q (2023). Genome editing for early and late flowering in plants. Bulletin Of Biological and Allied Sciences Research 1:45. https://doi.org/10.54112/bbasr.v2023i1.45

Jones DH (1984). Phenylalanine ammonia-lyase: regulation of its induction, and its role in plant development. Phytochemistry 23(7):1349-1359. https://doi.org/10.1016/S0031-9422(00)80465-3

Ju ZG, Yuan YB, Liou CL, Xin SH (1995). Relationship of phenylalanine ammonia lyase and anthocyanin synthesis in apple. Scientia Horticulturae 29(5):542b-542. https://doi.org/10.1016/0304-4238(94)00739-3

Kaur S, Samota MK, Choudhary M, Choudhary M, Pandey AK, Sharma A, Thakur J (2022). How do plants defend themselves against pathogens-Biochemical mechanisms and genetic interventions. Physiology and Molecular Biology of Plants 28(2):485-504. https://doi.org/10.1007/s12298-022-01146-y

Lam ML (1996). Phenylalanine ammonia-lyase (EC 4.3. 1.5) from Pinus banksiana: partial cDNA cloning and effect of exogenously supplied trans-cinnamic acid on elicitor-inducible expression. 1996, University of British Columbia.

Langenbacher AD, Shimizu H, Hsu W, Zhao Y, Borges A, Koehler C, Chen JN (2020). Mitochondrial calcium uniporter deficiency in zebrafish causes cardiomyopathy with arrhythmia. Frontiers in Physiology 11:617492. https://doi.org/10.3389/fphys.2020.617492

Li HG, Wang H, Cheng X, Su QX, Zhao Y, Jiang ST, Jin Q, Lin Y, Cai PY (2019). Genome-wide analysis of phenylalanine ammonia-lyase (PAL) gene family in five Rosaceae plants and expression analysis and functional identification of Chinese white pear. PeerJ Preprints 7:e27815v1. https://doi.org/10.7287/peerj.preprints.27815v1

Li WL, Faris JD, Chittoor JM, Leach JE, Hulbert SH, Liu DJ, Chen PD, Gill BS (1999). Genomic mapping of defense response genes in wheat. Theoretical and Applied Genetics 98:226-233. https://doi.org/10.1007/s001220051062

Liang XW, Dron M, Cramer CL, Dixon RA, Lamb CJ (1989). Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. Journal of Biological Chemistry 264(24):14486-92. https://doi.org/10.1016/S0021-9258(18)71704-3

Luo R, Pan W, Liu W, Tian Y, Zeng Y, Li Y, Li Z, Cui L (2022). The barley DIR gene family: An expanded gene family that is involved in stress responses. Frontiers in Genetics 13:1042772. https://doi.org/10.3389%2Ffgene.2022.1042772

Ma RF, Liu QZ, Xiao Y, Zhang L, Li Q, Yin J, Chen WS (2016). The phenylalanine ammonia-lyase gene family in Isatis indigotica Fort.: molecular cloning, characterization, and expression analysis. Chinese Journal of Natural Medicined 14(11):801-812. https://doi.org/10.1016/s1875-5364(16)30097-8

Magdy M, Mostofa MG, Rahimi M, Abd El Moneim D (2023). Editorial: Abiotic stress alleviation in plants: morpho-physiological and molecular aspects. Frontiers in Plant Science 14:1295638. https://doi.org/10.3389%2Ffpls.2023.1295638

Mattick JS (1994). Introns: evolution and function. Current Opinion in Genetics and Development 4(6): 823-31. https://doi.org/10.1016/0959-437x(94)90066-3

Mavandad M, Edwards R, Liang X, Lamb CJ, Dixon RA (1990). Effects of trans-cinnamic acid on expression of the bean phenylalanine ammonia-lyase gene family. Plant Physiology 94(2):671-80. https://doi.org/10.1104%2Fpp.94.2.671

Mazhar HSUD, Shafiq M, Ali H, Ashfaq M, Anwar A, Tabassum J, … Javed MA (2023). Genome-wide identification, and in-silico expression analysis of YABBY gene family in response to biotic and abiotic stresses in potato (Solanum tuberosum). Genes 14:824. https://doi.org/10.3390/genes14040824

Murale DP, Hong SC, Haque MM, Lee JS (2017). Photo-affinity labeling (PAL) in chemical proteomics: a handy tool to investigate protein-protein interactions (PPIs). Proteome Science 15:14. https://doi.org/10.1186/s12953-017-0123-3

Ngumbi E, Dady E, Calla B (2022). Flooding and herbivory: the effect of concurrent stress factors on plant volatile emissions and gene expression in two heirloom tomato varieties. BMC Plant Biology 22(1):536. https://doi.org/10.1186/s12870-022-03911-3

Owji H, Hemmati S (2018). A comprehensive in silico characterization of bacterial signal peptides for the excretory production of Anabaena variabilis phenylalanine ammonia lyase in Escherichia coli. 3 Biotech 8:1-15. https://doi.org/10.1016/0304-4238(94)00739-3

Patel ZM, Mahapatra R, Jampala SSM (2020). Role of fungal elicitors in plant defense mechanism. In: Molecular Aspects of Plant Beneficial Microbes in Agriculture. Elsevier, pp 143-158. https://doi.org/10.1016/B978-0-12-818469-1.00012-2

Pervaiz T, Songtao J, Faghihi F, Haider MS, Fang J (2017). Naturally occurring anthocyanin, structure, functions and biosynthetic pathway in fruit plants. Journal of Plant Biochemistry and Physiology 5:187. https://doi:10.4172/2329-9029.1000187

Rana V, Aashima B, Ravi S, Amit R, Priyanka (2022). Powdery mildew of wheat: research progress, opportunities, and challenges. New Horizons in Wheat and Barley Research: Crop Protection and Resource Management 133-178. https://doi.org/10.1007%2F978-981-16-4134-3_5

Rasool F, Uzair M, Naeem MK, Rehman N, Afroz A, Shah H, Khan MR (2021). Phenylalanine Ammonia-Lyase (PAL) genes family in wheat (Triticum aestivum L.): genome-wide characterization and expression profiling. Agronomy 11:2511. https://doi.org/10.3390/agronomy11122511

Rehman OU, Uzair M, Chao H, Fiaz S, Khan MR, Chen M (2022). Role of the type-B authentic response regulator gene family in fragrant rice under alkaline salt stress. Physiologia Plantarum 174(3):e13696. https://doi.org/10.1111/ppl.13696

Sami A, Haider MZ, Shafiq M, Sadiq S, Ahmad F (2024). Genome-wide identification and in-silico expression analysis of CCO gene family in sunflower (Helianthus annnus) against abiotic stress. Plant Molecular Biology 114(2):34. https://doi.org/10.1007/s11103-024-01433-0

Sami A, Haider, MZ, Shafiq M (2024). Microbial nanoenzymes: Features and applications, in Fungal Secondary Metabolites, Elsevier, pp 353-367. https://doi.org/10.1016/B978-0-323-95241-5.00015-0

Schluttenhofer CM (2011). The role of Arabidopsis mediator complex in plant defense. Purdue University. https://docs.lib.purdue.edu/dissertations/AAI10159589/

Sharma Poudel R, Richards J, Shrestha S, Solanki S, Brueggeman R (2019). Transcriptome-wide association study identifies putative elicitors/suppressor of Puccinia graminis f. sp. tritici that modulate barley rpg4-mediated stem rust resistance. BMC Genomics 20(1):985. https://doi.org/10.1186/s12864-019-6369-7

Smil V (2001). Feeding the world: A challenge for the twenty-first century. MIT press. https://mitpress.mit.edu/9780262692717/feeding-the-world/

Sun G (2012). MicroRNAs and their diverse functions in plants. Plant Molecular Biology 80(1):17-36. https://doi.org/10.1007/s11103-011-9817-6

Ullrich SE (2014). The Barley Crop: Origin and Taxonomy. Barley: Chemistry and Technology 1. http://dx.doi.org/10.1016/B978-1-891127-79-3.50001-9

Walker KR (2011). Regulation of candidate genes in black point formation in barley. (Doctoral thesis). The University of Adelaide, Adelaide, SA, Australia. https://hdl.handle.net/2440/80033

Wang X, Zhang Y, Zhang H, Qin G, Lin Q (2019). Complete mitochondrial genomes of eight seahorses and pipefishes (Syngnathiformes: Syngnathidae): insight into the adaptive radiation of Syngnathidae fishes. BMC Ecology and Evolution 19:119. https://doi.org/10.1186/s12862-019-1430-3

Weisshaar B, Jenkins GI (1998). Phenylpropanoid biosynthesis and its regulation. Current Opinion in Plant Biology 1(3):251-257. https://doi.org/10.1016/s1369-5266(98)80113-1

Whetten R, Sederoff R (1995). Lignin biosynthesis. The Plant Cell 7(7):1001. https://doi.org/10.1105/tpc.7.7.1001

Xu F, Deng G, Cheng S, Zhang W, Huang X, Li L, Cheng H, Rong X, Li J (2012). Molecular cloning, characterization and expression of the phenylalanine ammonia-lyase gene from Juglans regia. Molecules 17(7):7810-7823. https://doi.org/10.3390/molecules17077810

Yadav V, Wang Z, Wei C, Amo A, Ahmed B, Yang X, Zhang X (2020). Phenylpropanoid pathway engineering: An emerging approach towards plant defense. Pathogens 9(4):312. https://doi.org/10.3390%2Fpathogens9040312

Yu XZ, Fan WJ, Lin YJ, Zhang FF, Gupta DK (2018). Differential expression of the PAL gene family in rice seedlings exposed to chromium by microarray analysis. Ecotoxicology 27(3):325-335. https://doi.org/10.1007/s10646-018-1897-5

Zhan C, Li Y, Li H, Wang M, Gong S, Ma D, Li Y (2022). Phylogenomic analysis of phenylalanine ammonia-lyase (PAL) multigene family and their differential expression analysis in wheat (Triticum aestivum L.) suggested their roles during different stress responses. Frontiers in Plant Science 13:982457. https://doi.org/10.3389/fpls.2022.982457

Zhang F, Wang J, Li X, Zhang J, Liu Y, Chen Y, Yu Q, Li N (2023). Genome-wide identification and expression analyses of phenylalanine ammonia-lyase gene family members from tomato (Solanum lycopersicum) reveal their role in root-knot nematode infection. Frontiers in Plant Science 14:1204990. https://doi.org/10.3389%2Ffpls.2023.1204990

Zhang G, Li C (2010). Genetics and improvement of barley malt quality. Springer Science & Business Media. https://link.springer.com/book/10.1007/978-3-642-01279-2

Zhang XH, Liu HQ, Guo QW, Zheng CF, Li CS, Xiang XM, … Wan HJ (2016). Genome-wide identification, phylogenetic relationships, and expression analysis of the carotenoid cleavage oxygenase gene family in pepper. Genetics and Molecular Research 15(4). https://doi.org/10.4238/gmr.15048695

Downloads

Published

2024-09-12

How to Cite

ALBALAWI, T. (2024). Unraveling barley’s PAL gene family: a genome-wide study on defense mechanisms against Puccinia graminis f. sp. tritici. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(3), 13854. https://doi.org/10.15835/nbha52313854

Issue

Section

Research Articles
CITATION
DOI: 10.15835/nbha52313854