Please wait a minute...
Journal of Integrative Agriculture  2023, Vol. 22 Issue (5): 1351-1365    DOI: 10.1016/j.jia.2022.08.024
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Late sowing enhances lodging resistance of wheat plants by improving the biosynthesis and accumulation of lignin and cellulose
DONG Xiu-chun1, 2, QIAN Tai-feng1, CHU Jin-peng1, ZHANG Xiu1, LIU Yun-jing1, DAI Xing-long1#, HE Ming-rong1#

1 State Key Laboratory of Crop Biology, Ministry of Science and Technology/Key Laboratory of Crop Ecophysiology and Farming System, Ministry of Agriculture and Rural Affairs/Agronomy College, Shandong Agricultural University, Tai’an 271018, P.R.China

2 Jining Agricultural Technology Extension Center, Jining 272113, P.R.China

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  推迟播期利于提高小麦抗倒伏能力,但其内在机制尚不明确。本研究以冬小麦品种泰农18为供试材料,于2015–2016和2016–2017连续两个生长季进行大田试验,设置10月8日(常规播期)和10月22日(推迟播期)2个播期,旨在明确播期对木质素和纤维素代谢、茎秆形态特征、抗倒伏性能和产量的影响。结果表明,推迟播期通过促进茎秆中木质素和纤维素的合成与积累提高小麦抗倒伏能力。与常规播期相比,推迟播期促进木质素和纤维素合成相关基因(TaPALTaCCRTaCOMTTaCADTaCesA13478)表达水平和酶(TaPAL和TaCAD)活性水平提前4–12天到达相应峰值,并在大多数取样期显著提高除TaPALTaCCRTaCesA1和TaPAL之外的上述基因表达与酶活性水平,进而促进木质素和纤维素在茎秆伸长期的快速积累。木质素和纤维素的平均积累速率和最大积累速率越高,其最大积累量越多,纤维素的积累持续期也相应延长,拔节期及之后的茎秆木质素/纤维素比值、木质素含量以及拔节后11天的纤维素含量得以提高。进一步的研究表明,促进木质素和纤维素的合成与积累能够有效提高茎秆充实度、机械强度和抗倒伏性。然而,推迟播期增强小麦抗倒伏性能的关键功能基因有待进一步确定。


Delayed sowing mitigates lodging in wheat.  However, the mechanism underlying the enhanced lodging resistance in wheat has yet to be fully elucidated.  Field experiments were conducted to investigate the effects of sowing date on lignin and cellulose metabolism, stem morphological characteristics, lodging resistance, and grain yield.  Seeds of Tainong 18, a winter wheat variety, were sown on October 8 (normal sowing) and October 22 (late sowing) during both of the 2015–2016 and 2016–2017 growing seasons.  The results showed that late sowing enhanced the lodging resistance of wheat by improving the biosynthesis and accumulation of lignin and cellulose.  Under late sowing, the expression levels of key genes (TaPAL, TaCCR, TaCOMT, TaCAD, and TaCesA1, 3, 4, 7, and 8) and enzyme activities (TaPAL and  TaCAD) related to lignin and cellulose biosynthesis peaked 4–12 days earlier, and except for the TaPAL, TaCCR, and TaCesA1 genes and TaPAL, in most cases they were significantly higher than under normal sowing.  As a result, lignin and cellulose accumulated quickly during the stem elongation stage.  The mean and maximum accumulation rates of lignin and cellulose increased, the maximum accumulation contents of lignin and cellulose were higher, and the cellulose accumulation duration was prolonged.  Consequently, the lignin/cellulose ratio and lignin content were increased from 0 day and the cellulose content was increased from 11 days after jointing onward.  Our main finding is that the improved biosynthesis and accumulation of lignin and cellulose were responsible for increasing the stem-filling degree, breaking strength, and lodging resistance.  The major functional genes enhancing lodging resistance in wheat that are induced by delayed sowing need to be determined.

Keywords:  cellulose        late sowing       lignin       lodging resistance       wheat  
Received: 22 February 2022   Accepted: 22 April 2022

This work was supported by the National Key Research and Development Program of China (2016YFD0300403), the National Natural Science Foundation of China (31801298) and the Fund of Shandong ‘Double Top’ Program, China (SYL2017YSTD05).

About author:  DONG Xiu-chun, E-mail:; #Correspondence DAI Xing-long, E-mail:; HE Ming-rong, E-mail:

Cite this article: 

DONG Xiu-chun, QIAN Tai-feng, CHU Jin-peng, ZHANG Xiu, LIU Yun-jing, DAI Xing-long, HE Ming-rong. 2023. Late sowing enhances lodging resistance of wheat plants by improving the biosynthesis and accumulation of lignin and cellulose. Journal of Integrative Agriculture, 22(5): 1351-1365.

Acreche M M, Slafer G A. 2011. Lodging yield penalties as affected by breeding in Mediterranean wheats. Field Crops Research, 122, 40–48.
Ahmad I, Ahmad S, Yang X, Meng X, Yang B, Liu T, Han Q. 2021. Effect of uniconazole and nitrogen level on lodging resistance and yield potential of maize under medium and high plant density. Plant Biology, 23, 485–496.
Ahmad I, Kamran M, Ali S, Bilegjargal B, Cai T, Ahmad S, Meng X, Su W, Liu T, Han Q. 2018. Uniconazole application strategies to improve lignin biosynthesis, lodging resistance and production of maize in semiarid regions. Field Crops Research, 222, 66–77.
Ahmad I, Meng X, Kamran M, Ali S, Ahmad S, Liu T, Cai T, Han Q. 2020. Effects of uniconazole with or without micronutrient on the lignin biosynthesis, lodging resistance, and winter wheat production in semiarid regions. Journal of Integrative Agriculture, 19, 62–77.
Appenzeller L, Doblin M, Barreiro R, Wang H, Niu X, Kollipara K, Carrigan L, Tomes D, Chapman M, Dhugga S. 2004. Cellulose synthesis in maize: Isolation and expression analysis of the cellulose synthase (CesA) gene family. Cellulose, 11, 287–299.
Baldwin L, Głazowska S, Mravec J, Fangel J, Zhang H, Felby C, Willats W G, Schjoerring J K. 2017. External nitrogen input affects pre- and post-harvest cell wall composition but not the enzymatic saccharification of wheat straw. Biomass and Bioenergy, 98, 70–79.
Bi C, Chen F, Jackson L, Gill B S, Li W. 2011. Expression of lignin biosynthetic genes in wheat during development and upon interaction by fungal pathogens. Plant Molecular Biology Reporter, 29, 149–161.
Bremner J M. 1960. Determination of nitrogen in soil by the Kjeldahl method. Journal of Agricultural Science, 55, 11–33.
Chen C, Chang J, Wang S, Lu J, Liu Y, Si H, Sun G, Ma C. 2021. Cloning, expression analysis and molecular marker development of cinnamyl alcohol dehydrogenase gene in common wheat. Protoplasma, 258, 881–889.
Chen J, Lv F, Liu J, Ma Y, Wang Y, Chen B, Meng Y, Zhou Z. 2014. Effect of late planting and shading on cellulose synthesis during cotton fiber secondary wall development. PLoS ONE, 9, e105088.
Chen X G, Shi C Y, Yin Y P, Wang Z L, Shi Y H, Peng D L, Ni Y L, Cai T. 2011. Relationship between lignin metabolism and lodging resistance in wheat. Acta Agronomica Sinica, 37, 1616–1622. (in Chinese)
Dai X, Wang Y, Dong X, Qian T, Yin L, Dong S, Chu J, He M. 2017. Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat. The Crop Journal, 5, 541–552.
Desprez T, Juraniec M, Crowell E F, Jouy H, Pochylova Z, Parcy F, Höfte H, Gonneau M, Vernhettes S. 2007. Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 104, 15572–15577.
Domon J M, Baldwin L, Acket S, Caudeville E, Arnoult S, Zub H, Gillet F, Lejeune-Henaut I, Brancourt-Hulmel M, Pelloux J, Rayon C. 2013. Cell wall compositional modifications of Miscanthus ecotypes in response to cold acclimation. Phytochemistry, 85, 51–61.
Feng S W, Ru Z G, Ding W H, Hu T Z, Li G. 2019. Study of the relationship between field lodging and stem quality traits of winter wheat in the North China Plain. Crop and Pasture Science, 70, 772–780.
Hagiwara M, Izusawa H, Inoue N, Matano T. 1999. Varietal differences of shoot growth characters related to lodging in tartary buckwheat. Fagopyrum, 16, 67–72.
Hamann T, Osborne E, Youngs H L, Misson J, Nussaume L, Somerville C. 2004. Global expression analysis of CESA and CSL genes in Arabidopsis. Cellulose, 11, 279–286.
Houston K, Burton R A, Sznajder B, Rafalski A J, Dhugga K S, Mather D E, Taylor J, Steffenson B J, Waugh R, Fincher G B. 2015. A genome-wide association study for culm cellulose content in barley reveals candidate genes co-expressed with members of the CELLULOSE SYNTHASE A gene family. PLoS ONE, 10, e0130890.
Hu Y, Javed H H, Asghar M A, Peng X, Brestic M, Skalický M, Ghafoor A Z, Cheema H N, Zhang F, Wu Y. 2022. Enhancement of lodging resistance and lignin content by application of organic carbon and silicon fertilization in Brassica napus L. Frontiers in Plant Science, 13, 807048.
Kamran M, Ahmad I, Wu X, Liu T, Ding R, Han Q. 2018. Application of paclobutrazol: A strategy for inducing lodging resistance of wheat through mediation of plant height, stem physical strength, and lignin biosynthesis. Environmental Science and Pollution Research, 25, 29366–29378.
Kaur S, Dhugga K S, Gill K, Singh J. 2016. Novel structural and functional motifs in cellulose synthase (CesA) genes of bread wheat (Triticum aestivum L.). PLoS ONE, 11, e0147046.
Khobra R, Sareen S, Meena B K, Kumar A, Tiwar V, Singh G P. 2019. Exploring the traits for lodging tolerance in wheat genotypes: A review. Physiology and Molecular Biology of Plants, 25, 589–600.
Kong E, Liu D, Guo X, Yang W, Sun J, Li X, Zhang K, Cui D, Lin J, Zhang A. 2013. Anatomical and chemical characteristics associated with lodging resistance in wheat. The Crop Journal, 1, 43–49.
Kotake T, Aohara T, Hirano K, Sato A, Kaneko Y, Tsumuraya Y, Takatsuji H, Kawasaki S. 2011. Rice Brittle culm 6 encodes a dominant-negative form of CesA Protein that perturbs cellulose synthesis in secondary cell walls. Journal of Experimental Botany, 62, 2053–2062.
Li C, Luo Y, Jin M, Sun S, Wang Z, Li Y. 2021. Response of lignin metabolism to light quality in wheat population. Frontiers in Plant Science, 12, 729647.
Ma Q H. 2007. Characterization of a cinnamoyl-CoA reductase that is associated with stem development in wheat. Journal of Experimental Botany, 58, 2011–2021.
Ma Q H, Luo H R. 2015. Biochemical characterization of caffeoyl coenzyme A 3-O-methyltransferase from wheat. Planta, 242, 113–122.
McFarlane H E, Doring A, Persson S. 2014. The cell biology of cellulose synthesis. Annual Review of Plant Biology, 65, 69–94.
Melich A. 1953. Determination of P, Ca, Mg, K, Na, and NH4. North Carolina Soil Testing Division, NC State University, Raleigh, North Carolina, USA. pp. 23–89.
Morrison T A, Kessler J R, Hatfield R D, Buxton D R. 1994. Activity of two lignin biosynthesis enzymes during development of a maize internode. Journal of the Science of Food and Agriculture, 65, 133–139.
Niu L, Feng S, Ding W, Li G. 2016. Influence of speed and rainfall on large-scale wheat lodging from 2007 to 2014 in China. PLoS ONE, 11, e0157677.
Peake A S, Bell K L, Fischer R A, Gardner M, Das B T, Poole N, Mumford M. 2020. Cultivar × management interaction to reduce lodging and improve grain yield of irrigated spring wheat: Optimising plant growth regulator use, N application timing, row spacing and sowing date. Frontiers in Plant Science, 11, 401.
Peng D, Chen X, Yin Y, Lu K, Yang W, Tang Y, Wang Z. 2014. Lodging resistance of winter wheat (Triticum aestivm L.): Lignin accumulation and its related enzymes activities due to the application of paclobutrazol or gibberellin acid. Field Crops Research, 157, 1–7.
Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville C R. 2007. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 104, 15566–15571.
Shah A N, Tanveer M, Abbas A, Yildirim M, Shah A A, Ahmad M I, Wang Z, Sun W, Song Y. 2021. Combating dual challenges in maize under high planting density: Stem lodging and kernel abortion. Frontiers in Plant Science, 12, 699085.
Spink J H, Semere T, Sparkes D L, Whaley J M, Foulkes M J, Clare R W, Scott R K. 2005. Effect of sowing date on the optimum plant density of winter wheat. Annals of Applied Biology, 137, 179–188.
Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H. 2003. Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiology, 133, 73–83.
Turner S, Gallois P, Brown D. 2007. Tracheary element differentiation. Annals of Applied Biology, 58, 407–433.
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W. 2010. Lignin biosynthesis and structure. Plant Physiology, 153, 895–905.
Walkley A, Black I A. 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 37, 29–38.
Wang C, Hu D, Liu X B, She H Z, Ruan R W, Yang H, Yi Z L, Wu D Q. 2015a. Effects of uniconazole on the lignin metabolism and lodging resistance of culm in common buckwheat (Fagopyrum esculentum M.). Field Crops Research, 180, 46–53.
Wang C, Ruan R W, Yuan X H, Hu D, Yang H, Li Y, Yi Z L. 2015b. Effects of nitrogen fertilizer and planting density on the lignin synthesis in the culm in relation to lodging resistance of buckwheat. Plant Production Science, 18, 218–227.
Wang L, Guo K, Li Y, Tu Y, Hu H, Wang B, Cui X. 2010. Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biology, 10, 282.
Wang M, Zhu X, Wang K, Lu C, Luo M, Shan T, Zhang Z. 2018. A wheat caffeic acid 3-O-methltransferase TaCOMT-3D positively contributes to both resistance to sharp eyespot disease and stem mechanical strength. Scientific Reports, 8, 6543.
Weng F, Zhang W, Wu X, Xu X, Ding Y, Li G, Liu Z, Wang S. 2017. Impact of low-temperature, overcast and rainy weather during the reproductive growth stage on lodging resistance of rice. Scientific Reports, 7, 1–9.
Weng J K, Chapple C. 2010. The origin and evolution of lignin biosynthesis. New Phytologist, 187, 273–285.
Wu L, Zhang W, Ding Y, Zhang J, Camnula E D, Weng F, Liu Z, Ding C, Tang S, Chen L, Wang S, Li G. 2017. Shading contributes to the reduction of stem mechanical strength by decreasing cell wall synthesis in japonica rice (Oryza sativa L.). Frontiers in Plant Science, 8, 881.
Ye Y, Wang S, Wu K, Ren Y, Jiang H, Chen J, Tao L, Fu X, Liu B, Wu Y. 2021. A semi-dominant mutation in OsCESA9 improves salt tolerance and favors field straw decay traits by altering cell wall properties in rice. Rice, 14, 19.
Yin L, Dai X, He M. 2018. Delayed sowing improves nitrogen utilization efficiency in winter wheat without impacting yield. Field Crops Research, 221, 90–97.
Yu M, Wang M, Gyalpo T, Basang Y. 2021. Stem lodging resistance in hulless barley: Transcriptone and metabolome analysis of lignin biosynthesis pathways in contrasting genotypes. Genomics, 113, 935–943.
Yuen S H, Pollard A G. 1953. Determination of nitrogen in soil and plant materials: Use of boric acid in the micro-Kjeldahl method. Journal of the Science of Food and Agriculture, 4, 490–496.
Zandstra H G. 1968. Automated determination of phosphorus in sodium bicarbonate extracts. Canadian Journal of Soil Science, 48, 219–220.
Zhang J, Li G, Song Y, Liu Z, Yang C, Tang S, Zheng C, Wang S, Ding Y. 2014. Lodging resistance characteristics of high-yielding rice populations. Field Crops Research, 161, 64–74. 
Zhang M, Wang H, Yi Y, Ding J, Zhu M, Li C, Guo W, Feng C, Zhu X. 2017. Effect of nitrogen levels and nitrogen ratios on lodging resistance and yield potential of winter wheat (Triticum aestivum L.). PLoS ONE, 12, e0187543.
Zhang Q, Cheetamun R, Dhugga K S, Rafalski J A, Tingey S V, Shirley N J, Taylor J, Hayes K, Beatty M, Bacic A, Burton R A, Fincher G B. 2014. Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes. BMC Plant Biology, 14, 27.
Zhang R, Jia Z, Ma X, Ma H, Zhao Y. 2020. Characterising the morphological characters and carbohydrate metabolism of oat culms and their association with lodging resistance. Plant Biology, 22, 267–276.
Zhang W, Wu L, Ding Y, Weng F, Wu X, Li G, Liu Z, Tang S, Ding C, Wang S. 2016. Top-dressing nitrogen fertilizer rate contributes to decrease culm physical strength by reducing structural carbohydrate content in japonica rice. Journal of Integrative Agriculture, 15, 992–1004.
Zheng M, Chen J, Shi Y, Li Y, Yin Y, Yang D, Luo Y, Pang D, Xu X, Li W, Ni J, Wang Y, Wang Z, Li Y. 2017. Manipulation of lignin metabolism by plant densities and its relationship with lodging resistance in wheat. Scientific Reports, 7, 41805.
[1] CHU Jin-peng, GUO Xin-hu, ZHENG Fei-na, ZHANG Xiu, DAI Xing-long, HE Ming-rong. Effect of delayed sowing on grain number, grain weight, and protein concentration of wheat grains at specific positions within spikes[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2359-2369.
[2] FAN Ting-lu, LI Shang-zhong, ZHAO Gang, WANG Shu-ying, ZHANG Jian-jun, WANG Lei, DANG Yi, CHENG Wan-li. Response of dryland crops to climate change and drought-resistant and water-suitable planting technology: A case of spring maize[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2067-2079.
[3] DU Xiang-bei, XI Min, WEI Zhi, CHEN Xiao-fei, WU Wen-ge, KONG Ling-cong. Raised bed planting promotes grain number per spike in wheat grown after rice by improving spike differentiation and enhancing photosynthetic capacity[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1631-1644.
[4] WU Xian-xin, ZANG Chao-qun, ZHANG Ya-zhao, XU Yi-wei, WANG Shu, LI Tian-ya, GAO Li.

Characterization of wheat monogenic lines with known Sr genes and wheat cultivars for resistance to three new races of Puccinia graminis f. sp. tritici in China [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1740-1749.

[5] ZHANG Chong, WANG Dan-dan, ZHAO Yong-jian, XIAO Yu-lin, CHEN Huan-xuan, LIU He-pu, FENG Li-yuan, YU Chang-hao, JU Xiao-tang. Significant reduction of ammonia emissions while increasing crop yields using the 4R nutrient stewardship in an intensive cropping system[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1883-1895.
[6] ZHAO Xiao-dong, QIN Xiao-rui, LI Ting-liang, CAO Han-bing, XIE Ying-he. Effects of planting patterns plastic film mulching on soil temperature, moisture, functional bacteria and yield of winter wheat in the Loess Plateau of China[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1560-1573.
[7] ZHANG Zhen-zhen, CHENG Shuang, FAN Peng, ZHOU Nian-bing, XING Zhi-peng, HU Ya-jie, XU Fang-fu, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Effects of sowing date and ecological points on yield and the temperature and radiation resources of semi-winter wheat[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1366-1380.
[8] TIAN Xiao-min, HAN Peng, WANG Jing, SHAO Pan-xia, AN Qiu-shuang, Nurimanguli AINI, YANG Qing-yong, YOU Chun-yuan, LIN Hai-rong, ZHU Long-fu, PAN Zhen-yuan, NIE Xin-hui. Association mapping of lignin response to Verticillium wilt through an eight-way MAGIC population in Upland cotton[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1324-1337.
[9] LI Jiao-jiao, ZHAO Li, LÜ Bo-ya, FU Yu, ZHANG Shu-fa, LIU Shu-hui, YANG Qun-hui, WU Jun, LI Jia-chuang, CHEN Xin-hong. Development and characterization of a novel common wheat–Mexico Rye T1DL·1RS translocation line with stripe rust and powdery mildew resistance[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1291-1307.
[10] JIANG Yun, WANG De-li, HAO Ming, ZHANG Jie, LIU Deng-cai.

Development and characterization of wheat–Aegilops kotschyi 1Uk(1A) substitution line with positive dough quality parameters [J]. >Journal of Integrative Agriculture, 2023, 22(4): 999-1008.

[11] Sunusi Amin ABUBAKAR, Abdoul Kader Mounkaila HAMANI, WANG Guang-shuai, LIU Hao, Faisal MEHMOOD, Abubakar Sadiq ABDULLAHI, GAO Yang, DUAN Ai-wang. Growth and nitrogen productivity of drip-irrigated winter wheat under different nitrogen fertigation strategies in the North China Plain[J]. >Journal of Integrative Agriculture, 2023, 22(3): 908-922.
[12] TU Ke-ling, YIN Yu-lin, YANG Li-ming, WANG Jian-hua, SUN Qun. Discrimination of individual seed viability by using the oxygen consumption technique and headspace-gas chromatography-ion mobility spectrometry[J]. >Journal of Integrative Agriculture, 2023, 22(3): 727-737.
[13] TIAN Jin-yu, LI Shao-ping, CHENG Shuang, LIU Qiu-yuan, ZHOU Lei, TAO Yu, XING Zhi-peng, HU Ya-jie, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Increasing the appropriate seedling density for higher yield in dry direct-seeded rice sown by a multifunctional seeder after wheat-straw return[J]. >Journal of Integrative Agriculture, 2023, 22(2): 400-416.
[14] HU Wen-jing, FU Lu-ping, GAO De-rong, LI Dong-sheng, LIAO Sen, LU Cheng-bin. Marker-assisted selection to pyramid Fusarium head blight resistance loci Fhb1 and Fhb2 in a high-quality soft wheat cultivar Yangmai 15[J]. >Journal of Integrative Agriculture, 2023, 22(2): 360-370.
[15] Zaid CHACHAR, Siffat Ullah KHAN, ZHANG Xue-huan, LENG Peng-fei, ZONG Na, ZHAO Jun. Characterization of transgenic wheat lines expressing maize ABP7 involved in kernel development[J]. >Journal of Integrative Agriculture, 2023, 22(2): 389-399.
No Suggested Reading articles found!