Comparative transcript abundance of gibberellin oxidases genes in two barley (Hordeum vulgare) genotypes with contrasting lodging resistance under different regimes of water deficit
Shoaib Liaqat A , Zulfiqar Ali
A B C * , Muhammad Abu Bakar Saddique A , Rao Muhammad Ikram D and Imtiaz Ali E
A
B
C
D
E
Abstract
Barley (Hordeum vulgare) is the world’s fourth most important cereal crop, and is particularly well adapted to harsh environments. However, lodging is a major productivity constraint causing 13–65% yield losses. Gibberellic acid (GA) homeostatic genes such as HvGA20ox, HvGA3ox and HvGA2ox are responsible for changes in plant phenotype for height and internodal length that contribute towards lodging resistance. This study explored the expression of different HvGAox transcripts in two contrasting barley genotypes (5-GSBON-18, lodging resistant; and 5-GSBON-70, lodging sensitive), which were sown both under controlled (hydroponic, completely randomised factorial design) and field conditions (split-plot, completely randomised block design) with two irrigation treatments (normal with three irrigation events; and water deficit with one irrigation event). In the hydroponic experiment, expression analysis was performed on seedlings at 0, ¾, 1½, 3 and 6 h after application of treatment. In the field experiment, leaf, shoot nodes and internodes were sampled. Downregulation of HvGA20ox.1 transcript and 2-fold upregulation of HvGA2ox.2 transcript were observed in 5-GSBON-18 under water deficit conditions. This genotype also showed a significant reduction in plant height (18–20%), lodging (<10%), and increased grain yield (15–18%) under stress. Utilisation of these transcripts in barley breeding has the potential to reduce plant height, lodging and increased grain yield.
Keywords: barley, GA20ox, GA2ox, GA3ox, gibberellins, internodal length, lodging, plant height, transcript abundance, water stress.
References
Berry PM, Griffin JM, Sylvester-Bradley R, Scott RK, Spink JH, Baker CJ, Clare RW (2000) Controlling plant form through husbandry to minimise lodging in wheat. Field Crops Research 67(1), 59-81.
| Crossref | Google Scholar |
Berry PM, Kendall S, Rutterford Z, Orford S, Griffiths S (2015) Historical analysis of the effects of breeding on the height of winter wheat (Triticum aestivum) and consequences for lodging. Euphytica 203(2), 375-383.
| Crossref | Google Scholar |
Coles JP, Phillips AL, Croker SJ, García-Lepe R, Lewis MJ, Hedden P (1999) Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. The Plant Journal 17(5), 547-556.
| Crossref | Google Scholar | PubMed |
Cuesta-Marcos A, Casas AM, Hayes PM, Gracia MP, Lasa JM, Ciudad F, Codesal P, Molina-Cano JL, Igartua E (2009) Yield QTL affected by heading date in Mediterranean grown barley. Plant Breeding 128(1), 46-53.
| Crossref | Google Scholar |
Dockter C, Hansson M (2015) Improving barley culm robustness for secured crop yield in a changing climate. Journal of Experimental Botany 66(12), 3499-3509.
| Crossref | Google Scholar | PubMed |
Fischer RA, Stapper M (1987) Lodging effects on high-yielding crops of irrigated semidwarf wheat. Field Crops Research 17, 245-258.
| Crossref | Google Scholar |
Foster CE, Martin TM, Pauly M (2010) Comprehensive compositional analysis of plant cell walls (Lignocellulosic biomass) part I: lignin. Journal of Visualized Experiments e1745.
| Crossref | Google Scholar |
Gibson G, Weir B (2005) The quantitative genetics of transcription. Trends in Genetics 21(11), 616-623.
| Crossref | Google Scholar | PubMed |
He H, Liang G, Lu S, Wang P, Liu T, Ma Z, Zuo C, Sun X, Chen B, Mao J (2019) Genome-wide identification and expression analysis of GA2ox, GA3ox, and GA20ox are related to gibberellin oxidase genes in grape (Vitis Vinifera L.). Genes 10(9), 680.
| Crossref | Google Scholar | PubMed |
Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends in Plant Science 5(12), 523-530.
| Crossref | Google Scholar | PubMed |
Hyles J, Vautrin S, Pettolino F, MacMillan C, Stachurski Z, Breen J, Berges H, Wicker T, Spielmeyer W (2017) Repeat-length variation in a wheat cellulose synthase-like gene is associated with altered tiller number and stem cell wall composition. Journal of Experimental Botany 68(7), 1519-1529.
| Crossref | Google Scholar | PubMed |
Jia Q, Zhang J, Westcott S, Zhang X-Q, Bellgard M, Lance R, Li C (2009) GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley. Functional & Integrative Genomics 9(2), 255-262.
| Crossref | Google Scholar | PubMed |
Jia Q, Zhang X-Q, Westcott S, Broughton S, Cakir M, Yang J, Lance R, Li C (2011) Expression level of a gibberellin 20-oxidase gene is associated with multiple agronomic and quality traits in barley. Theoretical and Applied Genetics 122(8), 1451-1460.
| Crossref | Google Scholar | PubMed |
Jia Q, Li C, Shang Y, Zhu J, Hua W, Wang J, Yang J, Zhang G (2015) Molecular characterization and functional analysis of barley semi-dwarf mutant Riso no. 9265. BMC Genomics 16(1), 927.
| Crossref | Google Scholar |
Khalid MA, Ali Z, Tahir MHN, Ghaffar A, Ahmad J (2023) Genetic effects of GA-responsive dwarfing gene Rht13 on plant height, peduncle length, internodal length and grain yield of wheat under drought stress. Genes 14(3), 699.
| Crossref | Google Scholar |
Khobra R, Sareen S, Meena BK, Kumar A, Tiwari V, Singh GP (2019) Exploring the traits for lodging tolerance in wheat genotypes: a review. Physiology and Molecular Biology of Plants 25, 589-600.
| Crossref | Google Scholar | PubMed |
Kim SI, McKenzie KS, Tai TH (2009) A molecular survey of SD1 alleles used in U.S. rice cultivars. SABRAO Journal of Breeding and Genetics 41(1), 25-40.
| Google Scholar |
Kong E, Liu D, Guo X, Yang W, Sun J, Li X, Zhan K, Cui D, Lin J, Zhang A (2013) Anatomical and chemical characteristics associated with lodging resistance in wheat. The Crop Journal 1(1), 43-49.
| Crossref | Google Scholar |
Kuczyńska A, Surma M, Adamski T, Mikołajczak K, Krystkowiak K, Ogrodowicz P (2013) Effects of the semi-dwarfing sdw1/denso gene in barley. Journal of Applied Genetics 54, 381-390.
| Google Scholar | PubMed |
Liu L, Han R, Yu N, Zhang W, Xing L, Xie D, Peng D (2018) A method for extracting high-quality total RNA from plant rich in polysaccharides and polyphenols using Dendrobium huoshanense. PLoS ONE 13(5), e0196592.
| Crossref | Google Scholar | PubMed |
Nadeem M, Khan AA, Khan AA, Nadeem J, Fatima U (2023) Cloning and characterization of Trichoderma glucanase gene for plant transformation. International Journal of Agriculture and Biosciences 12(1), 31-46.
| Crossref | Google Scholar |
Okuno A, Hirano K, Asano K, Takase W, Masuda R, Morinaka Y, Ueguchi-Tanaka M, Kitano H, Matsuoka M (2014) New approach to increasing rice lodging resistance and biomass yield through the use of high gibberellin producing varieties. PLoS ONE 9(2), e86870.
| Crossref | Google Scholar | PubMed |
Olszewski N, Sun T-P, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. The Plant Cell 14, S61-S80.
| Crossref | Google Scholar | PubMed |
Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400(6741), 256-261.
| Crossref | Google Scholar | PubMed |
Peng D, Chen X, Yin Y, Lu K, Yang W, Tang Y, Wang Z (2014) Lodging resistance of winter wheat (Triticum aestivum L.): lignin accumulation and its related enzymes activities due to the application of paclobutrazol or gibberellin acid. Field Crops Research 157, 1-7.
| Crossref | Google Scholar |
Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L, Benlloch R, Nilsson O, Thomas SG, Hedden P, Phillips AL (2008) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. The Plant Cell 20(9), 2420-2436.
| Crossref | Google Scholar | PubMed |
Saddique MAB, Ali Z, Sher MA, Farid B, Ikram RM, Ahmad MS (2020) Proline, total antioxidant capacity, and OsP5CS gene activity in radical and plumule of rice are efficient drought tolerance indicator traits. International Journal of Agronomy 2020, 8862792.
| Crossref | Google Scholar |
Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K, Miyao A, Hirochika H, Kitano H, Ashikari M, Matsuoka M (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiology 134(4), 1642-1653.
| Crossref | Google Scholar | PubMed |
Shah L, Yahya M, Shah SMA, Nadeem M, Ali A, Ali A, Wang J, Riaz MW, Rehman S, Wu W, Khan RM, Abbas A, Riaz A, Anis GB, Si H, Jiang H, Ma C (2019) Improving lodging resistance: using wheat and rice as classical examples. International Journal of Molecular Sciences 20(17), 4211.
| Crossref | Google Scholar |
Shohat H, Cheriker H, Kilambi HV, Illouz Eliaz N, Blum S, Amsellem Z, Tarkowská D, Aharoni A, Eshed Y, Weiss D (2021) Inhibition of gibberellin accumulation by water deficiency promotes fast and long-term ‘drought avoidance’ responses in tomato. New Phytologist 232(5), 1985-1998.
| Crossref | Google Scholar | PubMed |
Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1),“green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proceedings of the National Academy of Sciences 99(13), 9043-9048.
| Crossref | Google Scholar |
Stamp P, Kiel C (1992) Root morphology of maize and its relationship to root lodging. Journal of Agronomy and Crop Science 168(2), 113-118.
| Crossref | Google Scholar |
Teshome S, Kebede M (2021) Analysis of regulatory elements in GA2ox, GA3ox and GA20ox gene families in Arabidopsis thaliana: an important trait. Biotechnology & Biotechnological Equipment 35(1), 1603-1612.
| Crossref | Google Scholar |
Tyagi K, Lee HJ, Lee CA, Steffenson BJ, Kim YJ, Yun SJ (2014) Variation in seedling root traits in wild barley (Hordeum vulgare L. ssp. spontaneum) germplasm. Plant Genetic Resources 12(S1), S79-S82.
| Crossref | Google Scholar |
Upadhya D, Dhakal R, Khadka K, Rana S, Acharya P, Rana R, Chaudhary P (2016) Local knowledge on climate-induced traits in rice for improving crop yield, food security and climate resilience. International Journal of Agriculture Innovations and Research 5, 385-396.
| Google Scholar |
Wang S, Wang Y (2022) Harnessing hormone gibberellin knowledge for plant height regulation. Plant Cell Reports 41(10), 1945-1953.
| Crossref | Google Scholar | PubMed |
Wu X, Wang Z, Chang X, Jing R (2010) Genetic dissection of the developmental behaviours of plant height in wheat under diverse water regimes. Journal of Experimental Botany 61, 2923-2937.
| Crossref | Google Scholar | PubMed |
Wu W, Shah F, Ma B-L (2022) Understanding of crop lodging and agronomic strategies to improve the resilience of rapeseed production to climate change. Crop and Environment 1, 133-144.
| Crossref | Google Scholar |
Yamaguchi S, Smith MW, Brown RGS, Kamiya Y, Sun T-P (1998) Phytochrome regulation and differential expression of gibberellin 3β-hydroxylase genes in germinating Arabidopsis seeds. The Plant Cell 10(12), 2115-2126.
| Crossref | Google Scholar | PubMed |
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Research 14(6), 415-421.
| Crossref | Google Scholar |
Zafar MM, Chattha WS, Khan AI, Zafar S, Subhan M, Saleem H, Ali A, Ijaz A, Anwar Z, Qiao F, Shakeel A, Seleiman MF, Wasonga DO, Parvaiz A, Razzaq A, Xuefei J (2023) Drought and heat stress on cotton genotypes suggested agro-physiological and biochemical features for climate resilience. Frontiers in Plant Science 14, 1265700.
| Crossref | Google Scholar | PubMed |
Zhang W, Wu L, Ding Y (2017) Nitrogen fertilizer application affects lodging resistance by altering secondary cell wall synthesis in japonica rice (Oryza sativa). Journal of Plant Research 130(5), 859-871.
| Crossref | Google Scholar | PubMed |
Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. The Plant Cell 18(2), 442-456.
| Crossref | Google Scholar | PubMed |
