转录组和代谢组分析揭示不同抗倒伏杂交小麦木质素合成积累的差异机制

doi:10.1016/j.jia.2023.06.027

摘要/Abstract

摘要：

杂交小麦应用是未来提高小麦产量的一种途径，当前部分杂交小麦品种株高的增加在一定程度上加大了其倒伏风险。本研究以两个抗倒伏性不同的杂交组合为试验材料，通过分析不同灌浆时期茎秆相关性状变化、基部第二节间转录组和代谢组数据及基部第二节间木质素合成积累等揭示其抗倒伏差异的形成机制。结果表明，抗倒伏杂交组合茎秆相关性状，如茎秆抗折力、穿刺强度、茎秆充实度及木质素含量（含G和S型单体）均显著高于倒伏敏感性组合。KEGG富集分析表明，灌浆后期差异代谢物和差异表达基因主要被显著富集到苯丙烷生物合成途径。本试验共鉴定了35个参与苯丙烷途径的关键调控基因，其中42%的基因在灌浆后期显著差异表达，且在显著差异表达基因中，超过80%的基因在抗倒伏组合中的表达显著高于其在倒伏敏感组合中的表达，而抗倒伏组合木质素合成途径中松柏醛、阿魏酸和松柏醇等中间代谢物显著低于倒伏敏感组合。综合分析表明，抗倒伏组合灌浆后期仍具有较高抗倒伏能力的关键在于其具有较高的木质素合成能力。本试验还通过对已审定杂交小麦和常规小麦品种的茎秆特征比较，提出了培育抗倒伏杂交小麦组合应关注的茎秆性状。

Abstract:

The use of hybrid wheat is one way to improve the yield in the future. However, greater plant heights increase lodging risk to some extent. In this study, two hybrid combinations with differences in lodging resistance were used to analyze the stem-related traits during the filling stage, and to investigate the mechanism of the difference in lodging resistance by analyzing lignin synthesis of the basal second internode (BSI). The stem-related traits such as the breaking strength, stem pole substantial degree (SPSD), and rind penetration strength (RPS), as well as the lignin content of the lodging-resistant combination (LRC), were significantly higher than those of the lodging-sensitive combination (LSC). The phenylpropanoid biosynthesis pathway was significantly and simultaneously enriched according to the transcriptomics and metabolomics analysis at the later filling stage. A total of 35 critical regulatory genes involved in the phenylpropanoid pathway were identified. Moreover, 42% of the identified genes were significantly and differentially expressed at the later grain-filling stage between the two combinations, among which more than 80% were strongly up-regulated at that stage in the LRC compared with LSC. On the contrary, the LRC displayed lower contents of lignin intermediate metabolites than the LSC. These results suggested that the key to the lodging resistance formation of LRC is largely the higher lignin synthesis at the later grain-filling stage. Finally, breeding strategies for synergistically improving plant height and lodging resistance of hybrid wheat were put forward by comparing the LRC with the conventional wheat applied in large areas.

Key words: gene expression , lignin synthesis , lodging-resistance , hybrid wheat

. 转录组和代谢组分析揭示不同抗倒伏杂交小麦木质素合成积累的差异机制[J]. Journal of Integrative Agriculture, 2024, 23(4): 1105-1117.

YANG Wei-bing, ZHANG Sheng-quan, HOU Qi-ling, GAO Jian-gang, WANG Han-Xia, CHEN Xian-Chao, LIAO Xiang-zheng, ZHANG Feng-ting, ZHAO Chang-ping, QIN Zhi-lie.

Transcriptomic and metabolomic analysis provides insights into lignin biosynthesis and accumulation and differences in lodging resistance in hybrid wheat [J]. Journal of Integrative Agriculture, 2024, 23(4): 1105-1117.

参考文献

Berry P M, Kendall S, Rutterford Z, Orford S, Griffiths S. 2014. Historical analysis of the effects of breeding on the height of winter wheat (Triticum aestivum L.) and consequences for lodging. Euphytica, 203, 375–383.

Berry P M, Sterling M, Spink J H, Baker C J, Mooney S J, Tams A R, Ennos A R. 2004. Understanding and reducing lodging in cereals. Advances in Agronomy, 18, 217–271.

Chabannes M, Ruel K, Yoshinaga A, Chabbert B, Jauneau A, Joseleau J P, Boudet A M. 2001. In situ analysis of lignins in transgenic tobacco reveals a differential impact of individual transformations on the spatial patterns of lignin deposition at the cellular and subcellular levels. The Plant Journal, 28, 271–282.

Chai L, Xin M, Dong C, Chen Z, Zhai H, Zhuang J, Cheng X, Wang N, Geng J, Wang X, Bian R, Yao Y, Guo W, Hu Z, Peng H, Bai G, Sun Q, Su Z, Liu J, Ni Z. 2022. A natural variation in Ribonuclease H-like gene underlies Rht8 to confer “Green Revolution” trait in wheat. Molecular Plant, 15, 377–380.

Chen J, Hu X, Shi T, Yin H, Sun D, Hao Y, Xia X, Luo J, Fernie A R, He Z, Chen W. 2020. Metabolite-based genome-wide association study enables dissection of the flavonoid decoration pathway of wheat kernels. Plant Biotechnology Journal, 18, 1722–1735.

Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X, Yu S, Xiong L, Luo J. 2013. A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: Application in the study of rice metabolomics. Molecular Plant, 6, 1769–1780.

Chen X, Wang J, Wang Z, Li W, Wang C, Yan S, Li H, Zhang A, Tang Z, Wei M. 2018. Optimized nitrogen fertilizer application mode increased culms lignin accumulation and lodging resistance in culms of winter wheat. Field Crops Research, 228, 31–38.

Dong X C, Qian T F, Chu J P, Zhang X, Liu Y J, Dai X L, He M R. 2023. Late sowing enhances lodging resistance of wheat plants by improving the biosynthesis and accumulation of lignin and cellulose. Journal of Integrative Agriculture, 22, 1351–1365.

Hai L, Guo H, Xiao S, Jiang G, Zhang X, Yan C, Xin Z, Jia J. 2005. Quantitative trait loci (QTL) of stem strength and related traits in a doubled-haploid population of wheat (Triticum aestivum L.). Euphytica, 141, 1–9.

Hou D, Lu H, Zhao Z, Pei J, Yang H, Wu A, Yu X, Lin X. 2022. Integrative transcriptomic and metabolomic data provide insights into gene networks associated with lignification in postharvest Lei bamboo shoots under low temperature. Food Chemistry, 368, 130822.

Hu D, Liu X B, She H Z, Gao Z, Ruan R W, Wu D Q, Yi Z L. 2017. The lignin synthesis related genes and lodging resistance of Fagopyrum esculentum. Biologia Plantarum, 61, 138–146.

Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou Y H, Yu J Q, Chen Z. 2010. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiology, 153, 1526–1538.

Huang X Q, Cloutier S, Lycar L, Radovanovic N, Humphreys D G, Noll J S, Somers D J, Brown P D. 2006. Molecular detection of QTLs for agronomic and quality traits in a doubled haploid population derived from two Canadian wheats (Triticum aestivum L.). Theoretical and Applied Genetics, 113, 753–766.

Islam M S, Peng S, Visperas R M, Ereful N, Bhuiya M S U, Julfiquar A W. 2007. Lodging-related morphological traits of hybrid rice in a tropical irrigated ecosystem. Field Crops Research, 101, 240–248.

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, 43–49.

Li B, Gao F, Ren B Z, Dong S T, Liu P, Zhao B, Zhang J W. 2021. Lignin metabolism regulates lodging resistance of maize hybrids under varying planting density. Journal of Integrative Agriculture, 20, 2077–2089.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2^–ΔΔCT method. Methods, 25, 402–408.

Longin C F, Muhleisen J, Maurer H P, Zhang H, Gowda M, Reif J C. 2012. Hybrid breeding in autogamous cereals. Theoretical and Applied Genetics, 125, 1087–1096.

Luo Y, Ni J, Pang D, Jin M, Chen J, Kong X, Li W, Chang Y, Li Y, Wang Z. 2019. Regulation of lignin composition by nitrogen rate and density and its relationship with stem mechanical strength of wheat. Field Crops Research, 241, 107572.

Ma Q H. 2009. The expression of caffeic acid 3-O-methyltransferase in two wheat genotypes differing in lodging resistance. Journal of Experimental Botany, 60, 2763–2771.

Ma Q H. 2010. Functional analysis of a cinnamyl alcohol dehydrogenase involved in lignin biosynthesis in wheat. Journal of Experimental Botany, 61, 2735–2744.

Mokochinski J B, Bataglion G A, Kiyota E, de Souza L M, Mazzafera P, Sawaya A C. 2015. A simple protocol to determine lignin S/G ratio in plants by UHPLC-MS. Analytical and Bioanalytical Chemistry, 407, 7221–7227.

Nakajima T, Yoshida M, Tomimura K. 2008. Effect of lodging on the level of mycotoxins in wheat, barley, and rice infected with the Fusarium graminearum species complex. Journal of General Plant Pathology, 74, 289–295.

Nguyen T N, Son S, Jordan M C, Levin D B, Ayele B T. 2016. Lignin biosynthesis in wheat (Triticum aestivum L.): its response to waterlogging and association with hormonal levels. BMC Plant Biology, 16, 28.

Ni F, Qi J, Hao Q, Lyu B, Luo M C, Wang Y, Chen F, Wang S, Zhang C, Epstein L, Zhao X, Wang H, Zhang X, Chen C, Sun L, Fu D. 2017. Wheat Ms2 encodes for an orphan protein that confers male sterility in grass species. Nature Communications, 8, 15121.

Ookawa T, Aoba R, Yamamoto T, Ueda T, Takai T, Fukuoka S, Ando T, Adachi S, Matsuoka M, Ebitani T, Kato Y, Mulsanti I W, Kishii M, Reynolds M, Pinera F, Kotake T, Kawasaki S, Motobayashi T, Hirasawa T. 2016. Precise estimation of genomic regions controlling lodging resistance using a set of reciprocal chromosome segment substitution lines in rice. Scientific Reports, 6, 30572.

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.

Shah A N, Tanveer M, Rehman A U, Anjum S A, Iqbal J, Ahmad R. 2017. Lodging stress in cereal-effects and management: An overview. Environmental Science and Pollution Research, 24, 5222–5237.

Shah L, Yahya M, Shah S M A, Nadeem M, Ali A, Ali A, Wang J, Riaz M W, Rehman S, Wu W, Khan R M, Abbas A, Riaz A, Anis G B, Si H, Jiang H, Ma C. 2019. Improving lodging resistance: Using wheat and rice as classical examples. International Journal of Molecular Sciences, 20, 4211.

Tian X, Xia X, Xu D, Liu Y, Xie L, Hassan M A, Song J, Li F, Wang D, Zhang Y, Hao Y, Li G, Chu C, He Z, Cao S. 2022. Rht24b, an ancient variation of TaGA2ox-A9, reduces plant height without yield penalty in wheat. New Phytologist, 233, 738–750.

Van De Velde K, Thomas S G, Heyse F, Kaspar R, Van Der Straeten D, Rohde A. 2021. N-terminal truncated RHT-1 proteins generated by translational reinitiation cause semi-dwarfing of wheat Green Revolution alleles. Molecular Plant, 14, 679–687.

Wang C, Hu D, Liu X, She H, Ruan R, Yang H, Yi Z, Wu D. 2015. 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, Yuan X, Hu D, Yang H, Li Y, Yi Z. 2014. Relationship between lignin metabolism and lodging resistance of culm in buckwheat. Journal of Agricultural Science, 6, 29–36.

Wang C Y, Dai X L, Shi Y H, Wang Z L, Chen X G, He M R. 2013. Effects of nitrogen application rate and plant density on lodging resistance in winter wheat. Acta Agronomica Sinica, 38, 121–128. (in Chinese)

Xiong H, Zhou C, Fu M, Guo H, Xie Y, Zhao L, Gu J, Zhao S, Ding Y, Li Y, Zhang J, Wang K, Li X, Liu L. 2022. Cloning and functional characterization of Rht8, a “Green Revolution” replacement gene in wheat. Molecular Plant, 15, 373–376.

Xiong S, Zuo X, Zhu Y. 2005. Determination of cellulose hemi-cellulose and ligin in rice hull. Cereal Feed Industry, 8, 40–41.

Yang W B, Qin Z L, Sun H, Hou Q L, Gao J G, Chen X C, Zhang L P, Wang Y B, Zhao C P, Zhang F T. 2022. Analysis of combining ability for stem-related traits and its correlations with lodging resistance heterosis in hybrid wheat. Journal of Integrative Agriculture, 21, 26–35.

Yao T, Feng K, Xie M, Barros J, Tschaplinski T J, Tuskan G A, Muchero W, Chen J G. 2021. Phylogenetic occurrence of the phenylpropanoid pathway and lignin biosynthesis in plants. Frontiers in Plant Science, 12, 704697.

Yin N, Li B, Liu X, Liang Y, Lian J, Xue Y, Qu C, Lu K, Wei L, Wang R, Li J, Chai Y. 2022. Two types of cinnamoyl-CoA reductase function divergently in accumulation of lignins, flavonoids and glucosinolates and enhance lodging resistance in Brassica napus. The Crop Journal, 10, 647–660.

Yu M, Wang M, Gyalpo T, Basang Y. 2021. Stem lodging resistance in hulless barley: Transcriptome and metabolome analysis of lignin biosynthesis pathways in contrasting genotypes. Genomics, 113, 935–943.

Zadoks J C, Chang T T, Konzak C F. 1974. A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.

Zhang H J, Li T, Liu H W, Mai C Y, Yu G J, Li H L, Yu L Q, Meng L Z, Jian D W, Yang L, Li H J, Zhou Y. 2020. Genetic progress in stem lodging resistance of the dominant wheat cultivars adapted to Yellow-Huai River Valleys Winter Wheat Zone in China since 1964. Journal of Integrative Agriculture, 19, 438–448.

Zhang P, Yan Y, Gu S, Wang Y, Xu C, Sheng D, Li Y, Wang P, Huang S. 2022. Lodging resistance in maize: A function of root–shoot interactions. European Journal of Agronomy, 132, 126393.

Zhang Q, Zhang L, Zhang L, Guo Y, Zhang D. 2007. Trendency on methods of high yield breeding of wheat. Journal of Triticeae Crops, 27, 176–178. (in Chinese)

Zhang X, Jia H, Li T, Wu J, Nagarajan R, Lei L, Powers C, Kan C C, Hua W, Liu Z, Chen C, Brett F C, Yan L. 2022. TaCol-B5 modifies spike architecture and enhances grain yield in wheat. Science, 376, 180–183.

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.