Please wait a minute...
Journal of Integrative Agriculture  2025, Vol. 24 Issue (12): 4528-4545    DOI: 10.1016/j.jia.2024.03.032
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Pod-shattering characteristic differences between shattering-resistant and shattering-susceptible common vetch accessions are associated with lignin biosynthesis
Xueming Dong, Jiwei Chen, Qiang Zhou, Dong Luo, Longfa Fang, Wenxian Liu, Zhipeng Liu#

State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems/Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs/Engineering Research Center of Grassland Industry, Ministry of Education/College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730000, China

 Highlights 
Variations in pod phenotypes and shattering traits between shattering-resistant and -susceptible common vetch were investigated.
Transcriptome analysis identified structural genes involved in lignin biosynthesis in common vetch.
Lignin accumulation is a potential major driver of pod shattering in common vetch.
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  
箭筈豌豆是一种自花授粉的一年生豆科牧草,分布于世界各地。它具有广泛的适应性和高营养价值,常被用作牲畜饲料的重要蛋白质来源。然而,箭筈豌豆的荚果破裂严重限制了其产量。为了阐明箭筈豌豆荚果破裂的机制,我们选择了3个抗裂(SR)种质(B65、B135和B392)和3个易裂(SS)种质(L33、L170和L461)的荚皮进行转录组测序。在盛花期后5、10、15、20和25天的B135和L461箭筈豌豆荚皮中共鉴定到17190个差异表达基因(DEGs)。KEGG分析显示,“苯丙烷生物合成”是最显著富集的通路,并且在B135和L461荚皮中鉴定出40个与木质素生物合成相关的结构基因,并在两者之间差异表达。此外,我们分析了盛花期后15天的3个SR和3个SS箭筈豌豆种质荚皮的DEGs,大部分DEGs的功能与在B135和L461箭筈豌豆不同发育时期中鉴定的富集通路一致。SR种质的总木质素含量显著低于SS种质。本研究为揭示箭筈豌豆裂荚特性与木质素生物合成相关的分子调控机制奠定了基础,并为育种家进一步培育抗裂荚箭筈豌豆提供了可参考的功能基因。


Abstract  
The common vetch (Vicia sativa L.) is a self-pollinated annual forage legume that is widely distributed worldwide.  It has wide adaptability and high nutritional value and is commonly used as an important protein source for livestock feed.  However, pod shattering seriously limits the yield of common vetch.  To clarify the mechanism of pod shattering in common vetch, the pod walls of three shattering-resistant (SR) accessions (B65, B135, and B392) and three shattering-susceptible (SS) accessions (L33, L170, and L461) were selected for transcriptome sequencing.  A total of 17,190 differentially expressed genes (DEGs) were identified in the pod wall of B135 and L461 common vetch at 5, 10, 15, 20, and 25 days after anthesis.  Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that “phenylpropanoid biosynthesis” was the most significantly enriched pathway, and 40 structural genes associated with lignin biosynthesis were identified and differentially expressed in B135 and L461 common vetch.  We analysed the DEGs in the pod wall of three SR and three SS accessions at 15 days after anthesis, and most of the DEGs were consistent with the significant enrichment pathways identified in B135 and L461 common vetch.  The total lignin content of SR accessions was significantly lower than the SS accessions.  The present study lays a foundation for understanding the molecular regulatory mechanism of pod shattering related to lignin biosynthesis in common vetch and provides reference functional genes for breeders to further cultivate shattering-resistant common vetch varieties.
Keywords:  Vicia sativa L.       pod shattering       pod wall       transcriptome       lignin biosynthesis  
Received: 15 November 2023   Accepted: 17 January 2024 Online: 06 March 2024  
Fund: This research was supported by the Leading Scientist Project of Qinghai Province, China (2023-NK-147).
About author:  #Correspondence Zhipeng Liu, E-mail: lzp@lzu.edu.cn

Cite this article: 

Xueming Dong, Jiwei Chen, Qiang Zhou, Dong Luo, Longfa Fang, Wenxian Liu, Zhipeng Liu. 2025. Pod-shattering characteristic differences between shattering-resistant and shattering-susceptible common vetch accessions are associated with lignin biosynthesis. Journal of Integrative Agriculture, 24(12): 4528-4545.

Abd El-Moneim A M. 1993. Selection for non-shattering common vetch, Vicia sativa L. Plant Breeding110, 168–171.

Ballester P, Ferrandiz C. 2016. Shattering fruits: Variations on a dehiscent theme. Current Opinion in Plant Biology35, 68–75.

Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annual Review of Plant Biology54, 519–546.

Bonawitz N D, Chapple C. 2010. The genetics of lignin biosynthesis: Connecting genotype to phenotype. Annual Review of Genetics44, 337–363.

Buchfink B, Xie C, Huson D H. 2015. Fast and sensitive protein alignment using diamond. Nature Methods12, 59–60.

Christiansen L C, Degan F D, Ulvskov P, Borkhardt B. 2002. Examination of the dehiscence zone in soybean pods and isolation of a dehiscence-related endopolygalacturonase gene. Plant Cell and Environment25, 479–490.

Chu W, Liu J, Cheng H T, Li C, Fu L, Wang W X, Wang H, Hao M Y, Mei D D, Liu K D, Hu Q. 2022. A lignified-layer bridge controlled by a single recessive gene is associated with high pod-shatter resistance in Brassica napus L. The Crop Journal10, 638–646.

Davies G C, Bruce D M. 1997. Fracture mechanics of oilseed rape pods. Journal of Materials Science32, 5895–5899.

Dong D K, Yan L F, Dong R, Liu W X, Wang Y R, Liu Z P. 2017. Evaluation and analysis of pod dehiscence factors in shatter-susceptible and shatter-resistant common vetch. Crop Science57, 2770–2776.

Dong R, Dong D K, Luo D, Zhou Q, Chai X T, Zhang J Y, Xie W G, Liu W X, Dong Y, Wang Y R, Liu Z P. 2017. Transcriptome analyses reveal candidate pod shattering-associated genes involved in the pod ventral sutures of common vetch (Vicia sativa L.). Frontiers in Plant Science8, 649.

Dong R, Jahufer M Z, Dong D K, Wang Y R, Liu Z P. 2016. Characterization of the morphological variation for seed traits among 537 germplasm accessions of common vetch (Vicia sativa L.) using digital image analysis. New Zealand Journal of Agricultural Research59, 422–435.

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 Agriculture22, 1351–1365.

Dong Y, Wang Y Z. 2015. Seed shattering: From models to crops. Frontiers in Plant Science6, 476.

Dong Y, Yang X, Liu J, Wang B H, Liu B L, Wang Y Z. 2014. Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean. Nature Communications5, 3352.

Franke Q, McMichael C M, Meyer K, Shirley A M, Cusumano J C, Chapple C. 2000. Modified lignin in tobacco and poplar over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. The Plant Journal22, 223–234.

Funatsuki H, Suzuki M, Hirose A, Inaba H, Yamada T, Hajika M, Komatsu K, Katayama T, Sayama T, Ishimoto M, Fujino K. 2014. Molecular basis of a shattering resistance boosting global dissemination of soybean. Proceedings of the National Academy of Sciences of the United States of America111, 17797–17802.

Guo M W, Zhu L, Li H Y, Liu W P, Wu Z N, Wang C H, Liu L, Li Z Y, Li J. 2022. Mechanism of pod shattering in the forage legume Medicago ruthenicaPlant Physiology and Biochemistry185, 260–267.

Huang Y F, Gao X L, Nan Z B, Zhang Z X. 2017. Potential value of the common vetch (Vicia sativa L.) as an animal feedstuff: A review. Journal of Animal Physiology and Animal Nutrition101, 807–823.

Jia C L, Dong D K, Zhou Q, Searle I R, Liu Z P. 2021. Significant cell differences in pod ventral suture in shatter-resistant and shatter-susceptible common vetch accessions. Crop Science61, 1749–1759.

Jia J, Wang H, Cai Z D, Wei R Q, Huang J H, Xia Q J, Xiao X H, Ma Q B, Nian H, Cheng Y B. 2022. Identification and validation of stable and novel quantitative trait loci for pod shattering in soybean [Glycinemax (L.) Merr.]. Journal of Integrative Agriculture21, 3169–3184.

Jiang L Y, Ma X, Zhao S S, Tang Y Y, Liu F X, Gu P, Fu Y C, Zhu Z F, Cai H W, Sun C Q, Tan L B. 2019. The APETALA2-like transcription factor SUPERNUMERARY BRACT controls rice seed shattering and seed size. The Plant Cell31, 17–36.

Kang X, Cai J J, Chen Y X, Yan Y C, Yang S T, He R Q, Wang D, Zhu Y L. 2019. Pod-shattering characteristics differences between two groups of soybeans are associated with specific changes in gene expression. Functional and Integrative Genomics20, 201–210.

Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods12, 357–360.

Kuai J, Sun Y Y, Guo C, Zhao L, Zuo Q S, Wu J S, Zhou G S. 2017. Root-applied silicon in the early bud stage increases the rapeseed yield and optimizes the mechanical harvesting characteristics. Filed Crops Research200, 88–97.

Li C, Zhou A, Sang T. 2006. Rice domestication by reducing shattering. Science311, 1936–1939.

Li L F, Olsen K M. 2016. Chapter three-to have and to hold: Selection for seed and fruit retention during crop domestication. Current Topics in Developmental Biology119, 63–109.

Liljegren S J, Ditta G S, Eshed Y, Savidge B, Bowman J L, Yanofsky M F. 2000. SHATTERPROOF MADS-box genes control seed dispersal in ArabidopsisNature404, 766–770.

Liljegren S J, Roeder A H K, Kempin S A, Gremski K, Østergaard L, Guimil S, Reyes D K, Yanofsky M F. 2004. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell116, 843–853.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods25, 402–408.

Lo S, Parker T, Muñoz-Amatriaín M, Berny-Mier J C, Teran Y, Jernstedt J, Close T J, Gepts P. 2021. Genetic, anatomical, and environmental patterns related to pod shattering resistance in domesticated cowpea [Vigna unguiculata (L.) Walp]. Journal of Experimental Botany72, 6219–6229.

Meyer J, Shirley A M, Cusumano J C, Bell-Lelong D A, Chapple C. 1998. Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in ArabidopsisProceedings of the National Academy of Sciences of the United States of America95, 6619–6623.

Miller A J, Gross B L. 2011. From forest to field: Perennial fruit crop domestication. American Journal of Botany98, 1389–1414.

Mitsuda N, Ohme-Takagi M. 2008. NAC transcription factors NST1 and NST3 regulate pod shattering in a partially redundant manner by promoting secondary wall formation after the establishment of tissue identity. The Plant Journal56, 768–778.

Murgia M L, Attene G, Rodriguez M, Bitocchi E, Bellucci E, Fois D, Nanni L, Gioia T, Albani D M, Papa R, Rau D. 2017. A comprehensive phenotypic investigation of the ‘pod-shattering syndrome’ in common bean. Frontiers in Plant Science8, 251.

Muriira N G, Xu W, Muchugi A, Xu J C, Liu A Z. 2015. De novo sequencing and assembly analysis of transcriptome in the Sodom apple (Calotropis gigantea). BMC Genomics16, 23.

Ning J, He W, Wu L H, Chang L Q, Hu M, Fu Y C, Liu F X, Sun H Y, Gu P, Ndjiondjop M N, Sun C Q, Zhu Z F. 2023. The MYB transcription factor Seed Shattering 11 controls seed shattering by repressing lignin synthesis in African rice. Plant Biotechnology Journal21, 931–942.

Parker T A, Teran J C B M y, Palkovic A, Jernstedt J, Gepts P. 2020. Pod indehiscence is a domestication and aridity resilience trait in common bean. New Phytologist225, 558–570.

Pertea M, Pertea G M, Antonescu C M, Chang T C, Mendell J T, Salzberg S L. 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology33, 290–295.

Philbrook B D, Oplinger E S. 1989. Soybean field losses as influenced by harvest delays. Agronomy Journal81, 251–258.

Rau D, Murgia M L, Rodriguez M, Bellucci E, Fois D, Albani D, Nanni L, Gioia T, Santo D, Marcolungo L, Delledonne M, Attene G, Papa R. 2018. Genomic dissection of pod shattering in common bean: Mutations at nonorthologous loci at the basis of convergent phenotypic evolution under domestication of leguminous species. The Plant Journal97, 693–714.

Reddy M S S, Chen F, Shadle G, Jackson L, Aljoe H, Dixon R A. 2005. Targeted down-regulation of cytochrome P450 enzymes for forage quality improvement in alfalfa (Medicago sativa L.). Proceedings of the National Academy of Sciences of the United States of America102, 16573–16578.

Repkova J, Hofbauer J. 2009. Seed pod shattering in the genus Lotus and its overcoming. Czech Journal of Genetics and Plant Breeding45, 39–44.

Rippert P, Puyaubert J, Grisollet D, Derrier L, Matringe M. 2009. Tyrosine and phenylalanine are synthesized within the plastids in ArabidopsisPlant Physiology149, 1251–1260.

Rodríguez-Gacio M C, Nicolás C, Matilla A J. 2004. Cloning and analysis of a cDNA encoding an endo-polygalacturonase expressed during the desiccation period of the silique-valves of turnip-tops (Brassica rapa L. cv. Rapa). Journal of Plant Physiology161, 219–227.

Seo J H, Kang B K, Dhungana S K, Oh J H, Choi M S, Park J H, Shin S O, Kim H S, Baek I Y, Sung J S, Jung C S, Kim K S, Jun T H. 2020. QTL mapping and candidate gene analysis for pod shattering tolerance in soybean (Glycine max). Plants9, 1163.

Suanum W, Somta P, Kongjaimun A, Yimram T, Kaga A, Tomooka N, Takahashi Y, Srinives P. 2016. Co-localization of QTLs for pod fiber content and pod shattering in F2 and backcross populations between yardlong bean and wild cowpea. Molecular Breeding36, 1–11.

Tao Z S, Huang Y, Zhang L D, Wang X F, Liu G H, Wang H Z. 2017. BnLATE, a Cys2/His2-type zinc-finger protein, enhances silique shattering resistance by negatively regulating lignin accumulation in the silique walls of Brassica napusPLoS ONE12, e0168046.

Wang Y, Chantreau M, Sibout R, Hawkins S. 2013. Plant cell wall lignification and monolignol metabolism. Frontiers in Plant Science4, 220.

Watcharatpong P, Kaga A, Chen X, Somta P. 2020. Narrowing down a major QTL region conferring pod fiber contents in Yardlong Bean (Vigna unguiculata), a vegetable cowpea. Genes11, 363.

Xi H W, Nguyen V, Ward C, Liu Z P, Searle I R. 2022. Chromosome-level assembly of the common vetch (Vicia sativa) reference genome. Gigabyte2022, 1–19.

Yamada T, Funatsuki H, Hagihara S, Fujita S, Tanaka Y, Tsuji H. 2009. A major QTL, qPDH1, is commonly involved in shattering resistance of soybean cultivars. Breeding Science59, 435–440.

Yang C Y, Song J, Ferguson A C, Klisch D, Simpson K, Mo R, Taylor B, Mitsuda N, Wilson Z A. 2017. Transcription factor MYB26 is key to spatial specificity in anther secondary thickening formation. Plant Physiology175, 333–350.

Yang J H, Wang H Z. 2016. Molecular mechanisms for vascular development and secondary cell wall formation. Frontiers in Plant Science7, 356.

Yoon J, Cho L H, Antt H W, Koh H J, An G. 2017. KNOX protein OSH15 induces grain shattering by repressing lignin biosynthesis genes. Plant Physiology174, 312–325.

Zaman Q U, Chu W, Shi Y Q, Hao M Y, Mei D S, Batley J, Zhang B H, Li C, Hu Q. 2021. Characterization of SHATTERPROOF homoeologs and CRISPR-Cas9-mediated genome editing enhances pod-shattering resistance in Brassica napus L. CRISPR Journal4, 360–370.

Zhang J P, Singh A K. 2020. Genetic control and geo-climate adaptation of pod dehiscence provide novel insights into soybean domestication. G3 - Genes Genomes Genetics10, 545–554.

Zhang Q, Wang L H, Wang Z T, Zhang R T, Liu P, Liu M J, Liu Z G, Zhao Z H, Wang L L, Chen X, Xu H F. 2021. The regulation of cell wall lignification and lignin biosynthesis during pigmentation of winter jujube. Horticulture Research8, 238.

Zhang Y, Shen Y Y, Wu X M, Wang J B. 2016. The basis of pod dehiscence: Anatomical traits of the dehiscence zone and expression of eight pod shatter-related genes in four species of BrassicaceaeBiologia Plantarum60, 343–354.

Zhao Q. 2016. Lignification: Flexibility, biosynthesis and regulation. Trends in Plant Science21, 713–721.

Zhou Y, Lu D F, Li C Y, Luo J H, Zhu B F, Zhu J J, Shangguan Y Y, Wang Z X, Sang T, Zhou B, Han B. 2012. Genetic control of seed shattering in rice by the APETALA2 transcription factor shattering abortion1The Plant Cell24, 1034–1048.

[1] Xuehao Zhang, Qiuling Zheng, Yongjiang Hao, Yingying Zhang, Weijie Gu, Zhihao Deng, Penghui Zhou, Yulin Fang, Keqin Chen, Kekun Zhang. Physiology and transcriptome profiling reveal the drought tolerance of five grape varieties under high temperatures[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3055-3072.
[2] Shan Wang, Kailin Shi, Yufan Xiao, Wei Ma, Yiguo Hong, Daling Feng, Jianjun Zhao. The circadian clock shapes diurnal gene expression patterns linked to glucose metabolic processes in Chinese cabbage[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2155-2170.
[3] Xinyi Mao, Xuan Zhao, Zhi Luo, Ao He, Meng Yang, Mengjun Liu, Jin Zhao, Ping Liu. Transcriptome-based analysis of lignin accumulation in the regulation of fruit stone development and endocarp hardening in Chinese jujube[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2217-2228.
[4] Teame Gereziher Mehari, Marijana Skorić, Hui Fang, Kai Wang, Fang Liu, Tesfay Araya, Branislav Šiler, Dengbing Yao, Baohua Wang. Insights into the role of GhCYP and GhTPS in the gossypol biosynthesis pathway via a multiomics and functional-based approach in cotton[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1671-1687.
[5] Congrui Sun, Runze Wang, Jiaming Li, Xiaolong Li, Bobo Song, David Edwards, Jun Wu. Pan-transcriptome analysis provides insights into resistance and fruit quality breeding of pear (Pyrus pyrifolia)[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1813-1830.
[6] Jin Wang, Minghua Wei, Haiyan Wang, Changjuan Mo, Yingchun Zhu, Qiusheng Kong. A time-course transcriptome reveals the response of watermelon to low-temperature stress[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1786-1799.
[7] Yonghui Fan, Yue Zhang, Yu Tang, Biao Xie, Wei He, Guoji Cui, Jinhao Yang, Wenjing Zhang, Shangyu Ma, Chuanxi Ma, Haipeng Zhang, Zhenglai Huang.
Response of wheat to winter night warming based on physiological and transcriptome analyses
[J]. >Journal of Integrative Agriculture, 2025, 24(3): 1044-1064.
[8] Xiaochun Wei, Yuanlin Zhang, Yanyan Zhao, Weiwei Chen, Ujjal Kumar Nath, Shuangjuan Yang, Henan Su, Zhiyong Wang, Wenjing Zhang, Baoming Tian, Fang Wei, Yuxiang Yuan, Xiaowei Zhang. Mitotic pollen abnormalities are linked to Ogura cytoplasmic male sterility in Chinese cabbage (Brassica rapa L. ssp. pekinensis)[J]. >Journal of Integrative Agriculture, 2025, 24(3): 1092-1107.
[9] Yiying Li, Yuanyuan Hu, Bei Wang, Mengyao Lang, Shutang Zhou, Zhongxia Wu. Transcriptome-based analysis reveals chromatin remodeling in post-adult eclosion reconstruction of the insect fat body[J]. >Journal of Integrative Agriculture, 2025, 24(2): 668-679.
[10] Yang Wang, Chunhua Mu, Xiangdong Li, Canxing Duan, Jianjun Wang, Xin Lu, Wangshu Li, Zhennan Xu, Shufeng Sun, Ao Zhang, Zhiqiang Zhou, Shenghui Wen, Zhuanfang Hao, Jienan Han, Jianzhou Qu, Wanli Du, Fenghai Li, Jianfeng Weng. A genome-wide association study and transcriptome analysis reveal the genetic basis for the Southern corn rust resistance in maize[J]. >Journal of Integrative Agriculture, 2025, 24(2): 453-466.
[11] Xiuling Wang, Li Niu, Huaipan Liu, Xucun Jia, Yulong Zhao, Qun Wang, Yali Zhao, Pengfei Dong, Moubiao Zhang, Hongping Li, Panpan An, Zhi Li, Xiaohuan Mu, Yongen Zhang, Chaohai Li. Integrated transcriptomics and metabolomics analysis provide insights into the alleviation of waterlogging stress in maize by exogenous spermidine application[J]. >Journal of Integrative Agriculture, 2025, 24(12): 4546-4560.
[12] Dongming Liu, Jinfang Liang, Quanquan Liu, Yaxin Chen, Shixiang Duan, Dongling Sun, Huayu Zhu, Junling Dou, Huanhuan Niu, Sen Yang, Shouru Sun, Jianbin Hu, Luming Yang. The pseudo-type response regulator gene Clsc regulates rind stripe coloration in watermelon[J]. >Journal of Integrative Agriculture, 2025, 24(1): 147-160.
[13] Lijiao Ge, Weihao Miao, Kuolin Duan, Tong Sun, Xinyan Fang, Zhiyong Guan, Jiafu Jiang, Sumei Chen, Weimin Fang, Fadi Chen, Shuang Zhao. Comparative transcriptome analysis identifies key regulators of nitrogen use efficiency in chrysanthemum[J]. >Journal of Integrative Agriculture, 2025, 24(1): 176-195.
[14] Yuting Zhu, Yongli Wang, Yidong Wang, Guiping Zhao, Jie Wen, Huanxian Cui. Transcriptome analysis reveals steroid hormones biosynthesis pathway involved in abdominal fat deposition in broilers[J]. >Journal of Integrative Agriculture, 2024, 23(9): 3118-3128.
[15] Meixue Sun, Tong Li, Yingjie Liu, Kenneth Wilson, Xingyu Chen, Robert I. Graham, Xianming Yang, Guangwei Ren, Pengjun Xu. A dicistrovirus increases pupal mortality in Spodoptera frugiperda by suppressing protease activity and inhibiting larval diet consumption[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2723-2734.
No Suggested Reading articles found!