根际黄酮类化合物缓解玉米-大豆带状间作荫蔽对大豆结瘤的抑制作用

doi:10.1016/j.jia.2024.09.030

摘要/Abstract

摘要：

豆科植物根系产生的黄酮类化合物是作为诱导共生根瘤菌nod基因的信号分子。然而，间作系统中根系分泌物中的黄酮类化合物对间作大豆结瘤的促进作用尚不清楚。采用玉米-大豆带状间作，即种间间距30 cm(MS30)、45 cm(MS45)、60 cm(MS60)和单一大豆/玉米：SS/MM，以及根相互作用，即根无屏障（NB）和根聚乙烯塑料屏障（PB），进行了为期两年的田间试验，评价根分泌物中类黄酮与结瘤的关系。结果发现，大豆和玉米之间的根-根相互作用提高间作大豆的根瘤数和鲜重。这种增强作用随着种间距离的扩大而逐渐增加。NB大豆直径大于0.4cm的根瘤占比高于PB大豆。根瘤形成相关基因GmENOD40、GmNIN2b和GmEXPB2表达上调。此外，与单间作相比，间作条件下大豆根系的异黄酮分泌减少，玉米和大豆根系的类黄酮和黄酮醇分泌增加。玉米和大豆根际黄酮类差异代谢产物的分泌随根屏障的增加而下降。在根系相互作用下，GmCHS8和GmIFS1在大豆根系中表达上调，GmICHG表达下调。黄酮类化合物和黄酮醇类化合物大多与结节直径呈正相关。经玉米根系分泌物处理的不同基因型大豆的根瘤数、根瘤鲜重和直径大于0.2 cm的根瘤比例均有所增加，促进了固氮能力的提高。因此，玉米-大豆带状间作结合合理的间距，可增强地下根系互作的积极作用，提高间作大豆的结瘤和固氮能力。

Abstract:

The flavonoids produced by legume roots are signal molecules that induce nod genes for symbiotic rhizobium. Nevertheless, the promoting effects of flavonoids in root exudates in intercropping system on soybean nodulation are still unknown. A two years of field experiments was carried with maize soybean strip intercropping, i.e., the interspecific row spacing of 30 cm (MS30), 45 cm (MS45), 60 cm (MS60), and sole soybean/maize:SS/MM, and root interaction, i.e., root no barrier (NB) and root polythene-plastic barrier (PB), to evaluate relationships between flavonoids in root exudates and nodulation. We found that root-root interaction between soybean and maize enhances the nodules number and fresh weight in intercropped soybean. This enhancement increase gradually with expansion of interspecific distance. Proportion of nodules with diameter greater than 0.4cm was higher in intercropped soybean with NB than with PB. The expressions of nodules-related genes (GmENOD40, GmNIN2b and GmEXPB2) were up-regulated. Furthermore, compared with monocropping, isoflavones secretion of soybean roots reduced, flavonoids and flavonols secretion of maize and soybean roots increased under intercropping. The secretion of differential metabolites of flavonoids in the rhizosphere of maize and soybean declined with root barrier. The expressions of GmCHS8 and GmIFS1 in soybean roots were up-regulated and GmICHG was down-regulated under root interaction. The most of the flavonoids and flavonol compounds were positively correlated with nodule diameter. The nodules number, the nodules fresh weight and the proportion of nodules with a diameter greater than 0.2 cm increased in different genotypes of soybean treated with maize root exudate, which promoted the improvement of nitrogen fixation capacity. Therefore, maize-soybean strip intercropping combined with reasonable spacing to enhance the positive effect of underground root interaction, and improve the nodulation and nitrogen fixation capacity of intercropping soybean.

Key words: maize-soybean strip intercropping , root interaction , flavonoids , nodule

. 根际黄酮类化合物缓解玉米-大豆带状间作荫蔽对大豆结瘤的抑制作用[J]. Journal of Integrative Agriculture, DOI: 10.1016/j.jia.2024.09.030.

Ping Lin, Shanshan Liu, Zhidan Fu, Kai Luo, Yiling Li, Xinyue Peng, Xiaoting Yuan, Lida Yang, Tian Pu, Yuze Li, Taiwen Yong, Wenyu Yang. Rhizosphere flavonoids alleviates the inhibition of soybean nodulation caused by shading under maize-soybean strip intercropping[J]. Journal of Integrative Agriculture, DOI: 10.1016/j.jia.2024.09.030.

参考文献

Barcelo J, Poschenrieder C. 2022. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: A review. Environmental and Experimental Botany, 48, 75–92.

Brooker R W, Bennett A E, Cong W F, Daniell T J, George T S, Hallett P D, Hawes C, Iannetta P P M, Jones H G, Karley A J, Li L, McKenzie B M, Pakeman R J, Paterson E, Schöb C, Shen J B, Squire G, Watson C A, Zhang C C, Zhang F S, et al. 2015. Improving intercropping: A synthesis of research in agronomy, plant physiology and ecology. New Phytologist, 206, 107-117.

Chen L Y, Qin L, Zhou L L, Li X X, Chen Z C, Sun L L, Wang W F, Lin Z H, Zhao J, Yamaji N, Ma J F, Gu M, Xu G H, Liao H. 2018. A nodule-localized phosphate transporter GmPT7 plays an important role in enhancing symbiotic N₂ fixation and yield in soybean. New Phytologist, 221, 2013-2025.

Chen P, Du Q, Zheng B, Yang H, Fu Z, Luo K, Lin P, Li Y, Pu T, Yong T, Yang W. 2024. Coordinated responses of leaf and nodule traits contribute to the accumulation of N in relay intercropped soybean. Journal of Integrative Agriculture, 23, 1910-1928.

Fan F L, Zhang F S, Song Y N, Sun J H, Bao X G, Guo T W, Li L. 2006. Nitrogen fixation of faba bean (Vicia faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant and Soil, 283, 275–286.

Fu M D, Sun J F, Li X L, Guan Y F, Xie F. 2022. Asymmetric redundancy of soybean Nodule Inception (NIN) genes in root nodule symbiosis. Plant Physiology, 188, 477–489.

Gao Y, Duan A W, Qiu X Q, Liu Z G, Sun J S, Zhang J P, Wang H Z. 2010. Distribution of roots and root length density in a maize/soybean strip intercropping system. Agricultural Water Management, 98, 199-212.

Giordano W, Hirsch A M. 2004. The expression of MaEXP1, aMelilotus alba expansin gene, is upregulated during the sweetclover-Sinorhizobium meliloti interaction. Molecular Plant-Microbe Interactions, 17, 613–622.

Hazrati H, Fomsgaard I S, Kudsk P. 2020. Root-exuded benzoxazinoids: Uptake and translocation in neighboring plants. Journal of Agricultural and Food Chemistry, 68, 10609-10617.

Herridge D F, Peoples M B, Boddey R M. 2008. Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil, 311, 1–18.

Huang A C, Jiang T, Liu Y X, Bai Y C, Reed J, Qu B Y, Goossens A, Nützmann H W, Bai Y, Osbourn A. 2019. A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science, 364, 6389.

Huang X F, Chaparro J M, Reardon K F, Zhang R F, Shen Q R, Vivanco J M. 2014. Rhizosphere interactions: Root exudates, microbes, and microbial communities. Botany, 92, 267–275.

Indrasumunar A, Searle I, Lin M H, Kereszt A, Men A, Carroll B J, Gresshoff P M. 2011. Nodulation factor receptor kinase 1α controls nodule organ number in soybean (Glycine max L. Merr.). Plant Journal, 65, 39–50.

Ito S, Ohtake N, Sueyoshi K, Ohyama T. 2006. Allocation of photosynthetic products in soybean during the early stages of nodule formation. Journal of Soil Science and Plant Nutrition, 52, 438-443.

Jung W, Yu O, Lau S M C, O’Keefe D P, Odell J, Fader G, Mcgonigle B. 2000. Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes. Nature Biotechnology, 18, 208–212.

Li B, Li Y Y, Wu H M, Li L. 2016. Root exudates drive interspecific facilitation by enhancing nodulation and N₂ fixation. Proceedings of the National Academy of Sciences of the United States of America, 113, 6496-6501.

Li X X, Zhao J, Tan Z Y, Zeng R S, Liao H. 2015. GmEXPB2, a cell wall b-expansin, affects soybean nodulation through modifying root architecture and promoting nodule formation and development. Plant Physiology, 169, 2640-2653.

Li Y L, Chen P, Fu Z, Luo K, Lin P, Gao C, Liu S, Pu T, Yong T W, Yang W Y. 2023. Maize-soybean relay cropping increases soybean yield synergistically by extending the post-anthesis leaf stay-green period and accelerating grain filling. The Crop Journal, 11, 1921-1930.

Li Y Y, Yu C B, Cheng X, Li C J, Sun J H, Zhang F S, Lambers H, Li L. 2009. Intercropping alleviates the inhibitory effect of N fertilization on nodulation and symbiotic N₂ fixation of faba bean. Plant and Soil, 323, 295-308.

Li Y Z, Gu X Y, Yong T W, Yang W Y. 2024. A global synthesis reveals additive density design drives intercropping effects on soil N-cycling variables. Soil Biology and Biochemistry, 191, 109318.

Lian B, Souleimanov A, Zhou X, Smith D L. 2002. In vitro induction of lipo-chitooligosaccharide production in Bradyrhizobium japonicum cultures by root extracts from non-leguminous plants. Microbiological Research, 157, 157–160.

Liu H T, Chen S H, Li B G, Guo S, Tian J, Yao L, Lin C W. 2022. The effect of strip orientation and width on radiation interception in maize–soybean strip intercropping systems. Food and Energy Security, 11, e364.

Liu X, Rahman T, Song C, Su B, Yang F, Yong T W, Wu Y S, Zhang C Y, Yang W Y. 2017. Changes in light environment, morphology, growth and yield of soybean in maize-soybean intercropping systems. Field Crops Research, 200, 38–46.

Liu Y C, Qin X M, Xiao J X, Tang L, Wei C Z, Wei J J, Zheng Y. 2017. Intercropping influences component and content change of flavonoids in root exudates and nodulation of Faba bean. Journal of Plant Interactions, 12, 187–192.

Lyu X C, Sun C Y, Lin T, Wang X L, Li S, Zhao S H, Gong Z P, Wei Z W, Yan C, Ma C M. 2022. Systemic regulation of soybean nodulation and nitrogen fixation by nitrogen via isoflavones. Frontiers in Plant Science, 13, 968496.

Mulder L, Hogg B, Bersoult A, Cullimore J V. 2005. Integration of signalling pathways in the establishment of the legume-rhizobia symbiosis. Physiologia Plantarum, 123, 207–218.

Nguyen H P, Miwa H, Obirih-Opareh J, Suzaki T, Yasuda M, Okazaki S. 2019. Novel rhizobia exhibit superior nodulation and biological nitrogen fixation even under high nitrate concentrations. FEMS Microbiology Ecology, 96, fiz184.

Ohwakiy S. 1997. Active extrusion of protons and exudation of carboxylic acids in response to iron deficiency by roots of chickpea (Cicer arietinum L.). Plant and Soil, 189, 49-55.

Poole P, Ramachandran V, Terpolilli J. 2018. Rhizobia: From saprophytes to endosymbionts. Nature Reviews Microbiology, 16, 291-303.

Rao J R, Cooper J E. 1995. Soybean nodulating rhizobia modify nod gene inducers daidzein and genistein to yield aromatic products that can influence gene-inducing activity. Molecular Plant-Microbe Interactions, 8, 855-862.

Raza M A, Cui L, Khan I, Ud-Din A M, Chen G P, Ansar M, Manaf A, Titriku J K, Shah G A, Yang F, Yang W. 2021. Compact maize canopy improves radiation use efficiency and grain yield of maize/soybean relay intercropping system. Environmental Science and Pollution Research, 28, 41135–41148.

Raza M A, Cui L, Qin R J, Yang F, Yang W Y. 2020. Strip-width determines competitive strengths and grain yields of intercrop species in relay intercropping system. Scientific Reports, 10, 1-12.

Raza M A, Din A M U, Wang Z Q, Gul H, Ur Rehman S, Bukhari B, Haider I, Ur Rehman M H, Liang X, Luo S L, Sabagh A E, Qin R J, Ma Z M. 2023. Spatial differences influence nitrogen uptake, grain yield, and land-use advantage of wheat/soybean relay intercropping systems. Scientific Reports, 13, 16916.

Raza M A, Feng L Y, van der Werf W, Cai G R, Khalid M H B, Iqbal N, Hassan M J, Meraj T A, Naeem M, Khan I, ur Rehman S, Ansar M, Ahmed M, Yang F, Yang W Y. 2019a. Narrow-wide-row planting pattern increases the radiation use efficiency and seed yield of intercrop species in relay-intercropping system. Food and Energy Security, 8, e170.

Raza M A, Khalid M H B, Zhang X, Feng L Y, Khan I, Hassan M J, Ahmed M, Ansar M, Chen Y K, Fan Y F, Yang F, Yang W Y. 2019b. Effect of planting patterns on yield, nutrient accumulation and distribution in maize and soybean under relay intercropping systems. Scientific Reports, 9, 4947.

Roy S, Nandety R S, Crook A, Mysore K S, Pislariu C I, Frugoli J, Dickstein R, Udvardi M. 2020. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell, 32, 15-41.

Santelia D, Henrichs S, Vincenzetti V, Sauer M. 2008. Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. Journal of Biological Chemistry, 283, 31218-31226

Silva P T, Lima M F, Cruz L S, de Moraes R M, de Souza S R, Furlan C M. 2022. Alterations in the flavonoid pathway and VOCs confer photoprotection in UVB-irradiated soybean. Theoretical and Experimental Plant Physiology, 34, 551-562.

Sreevidya V, Rao C S, Sullia S, Ladha J K, Reddy P M. 2006. Metabolic engineering of rice with soybean isoflavone synthase for promoting nodulation gene expression in rhizobia. Journal of Experimental Botany, 57, 1957–1969.

Subramanian S, Stacey G, Yu O. 2006. Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant Journal, 48, 261–273.

Sugiyama A, Shitan N, Yazaki K. 2007. Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-Rhizobium symbiosis. Plant Physiology, 144, 2000–2008.

Sugiyama A, Yamazaki Y, Yamashita K, Takahashi S, Nakayama T, Yazaki K. 2016. Developmental and nutritional regulation of isoflavone secretion from soybean roots. Bioscience Biotechnology Biochemistry, 80, 89-94.

Sujkowska M, Borucki W, Golinowski W. 2007. Localization of expansinlike protein in apoplast of pea (Pisum sativum L.) root nodules during interaction with Rhizobium leguminosarum bv. viciae. Acta Societatis Botanicorum Poloniae, 76, 17–26.

Suzuki H, Takahashi S, Watanabe R, Fukushima Y, Fujita N, Noguchi A, Yokoyama R, Nishitani K, Nishino T, Nakayama T. 2006. An isoflavone conjugate-hydrolyzing beta-glucosidase from the roots of soybean (Glycine max) seedlings: Purification, gene cloning, phylogenetics, and cellular localization. Journal of Biological Chemistry, 281, 30251–30259.

Te X, Ud Din A M, Cui K, Raza M A, Ali M F, Xiao J H. 2023. Inter-specific root interactions and water use efficiency of maize/soybean relay strip intercropping, Field Crops Research, 291, 108793.

Wang C, Li M, Zhao Y, Liang N, Li H, Li P, Yang L, Xu M, Bian X, Wang M, Wu S, Niu X, Wang M, Li X, Sang Y, Dong W, Wang E, Gallagher K L, Wu S. 2022. Short-root paralogs mediate feedforward regulation of D-type cyclin to promote nodule formation in soybean. Proceedings of the National Academy of Sciences of the United States of America, 119, e2108641119.

Wasson A P, Pellerone F I, Mathesius U. 2006. Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell, 18, 1617–1629.

White L J, Ge X, Brozel V S, Subramanian S. 2017. Root isoflavonoids and hairy root transformation influence key bacterial taxa in the soybean rhizosphere. Environmental Microbiology, 19, 1391-1406.

Yan D, Tajima H, Cline L C, Fong R Y, Ottaviani J I, Shapiro H Y, Blumwald E. 2022. Genetic modification of flavone biosynthesis in rice enhances biofilm formation of soil diazotrophic bacteria and biological nitrogen fixation. Plant Biotechnology Journal, 20, 2135-2148.

Yang J, Lan L Y, Jin Y, Yu N, Wang D, Wang E T. 2022. Mechanisms underlying legume-rhizobium symbioses. Journal of Integrative Plant Biology, 64, 244-267.

Yong T W, Liu X M, Yang F, Shong C, Wang X C, Liu W G, Su B Y, Zhou L, Yang W Y. 2015. Characteristics of nitrogen uptake, use and transfer in a wheat-maize-soybean relay intercropping system. Plant Production Science, 18, 388-397.

Yu R P, Lambers H, Callaway R M, Wright A J, Li L. 2021. Belowground facilitation and trait matching: Two or three to tango? Trends in Plant Science, 26, 1227-1235.

Zhang Y, Sun Z X, Su Z C, Du G J, Bai W, Wang Q, Wang R, Nie J Y, Sun T, Feng C, Zhang Z, Yang N, Zhang X, B. Evers J, van der Werf W, Zhang L Z. 2022. Root plasticity and interspecific complementarity improve yields and water use efficiency of maize/soybean intercropping in a water-limited condition. Field Crops Research, 282, 108523.

Zhang Y Z, Wang E T, Li M, Li Q Q, Zhang Y M, Zhao S J, Jia X L, Zhang L H, Chen W F, Chen W X. 2011. Effects of rhizobial inoculation, cropping systems and growth stages on endophytic bacterial community of soybean roots. Plant and Soil, 347, 147–161.

Zheng B C, Zhou Y, Chen P, Zhang X N, Du Q, Yang H, Wang X C, Yang F, Xiao T, Li L, Yang W Y, Yong T W. 2022. Maize–legume intercropping promote N uptake through changing the root spatial distribution, legume nodulation capacity, and soil N availability. Journal of Integrative Agriculture, 21, 1755–1771.

Zhou T, Wang L, Yang H, Gao Y, Liu W G, Yang W Y. 2019. Ameliorated light conditions increase the P uptake capability of soybean in a relay-strip intercropping system by altering root morphology and physiology in the areas with low solar radiation. Science of the Total Environment, 688, 1069-1080.