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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (2): 353-366.doi: 10.3724/SP.J.1006.2022.14006

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Identification, expression profile of soybean PIN-Like (PILS) gene family and its function in symbiotic nitrogen fixation in root nodules

DONG Yan-Kun1(), HUANG Ding-Quan2, GAO Zhen2, CHEN Xu2,*()   

  1. 1College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, Fujian, China
    2Haixia Institute of Science and Technology, Horticultural Plant Biology and Metabolomics Center, Fujian Agriculture and Forestry University, Fuzhou 350002, Fujian, China
  • Received:2021-01-11 Accepted:2021-04-26 Online:2022-02-12 Published:2021-05-18
  • Contact: CHEN Xu E-mail:dongyk1124@163.com;chenxu@inbox.com
  • Supported by:
    This study was supported by the National Key Research and Development Program of China “Seven Major Crop Breeding” Special Topic Crop Organ Development and Nutrient Efficient Use Interaction Mechanism(2016YFD0100705)

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Abstract:

Plant hormone auxin plays a vital role in the growth and development of plants. Auxin homeostasis and concentration gradient establishment control the polar formation of almost all organs. The synthesis, transportation, perception, and metabolic degradation of auxin in specific cells establish a concentration gradient of auxin in accordance with organ development. In legumes, roots interact with soil microorganisms to form a special organ called nodules, which is used for biological nitrogen fixation. However, the function of auxin homeostasis control of biological nitrogen fixation is unknown. Studies showed that PIN-Like (PILS) proteins in Arabidopsis helped to regulate intracellular auxin homeostasis and mediate auxin signal transmission in the downstream nucleus. In this study, 19 PILS family genes (GmPILSs) were identified in soybean genome and distributed unevenly on 10 chromosomes of soybean. GmPILSs exhibited a variety of expression patterns in nine tissue parts of soybean, and had obvious specificity of tissue expression. GmPILS1e and GmPILS1f were enriched and expressed in the rhizobia region, and the expression of GmPILS1e and GmPILS1f in nodules was down-regulated by artificial microRNA interference (amiRNAi), resulting in the increase of nitrogenase activity in the nodules. However, the overexpression of GmPILS1f leaded to the decrease nitrogenase activity in root nodules, GmPILS1e and GmPILS1f might participate in the regulation of soybean nitrogenase activity. These results lay the foundation for further analysis of the function and mechanism of soybean GmPILS family genes, and also provide valuable genetic resources for the application of nodulation and nitrogen fixation in agricultural breeding.

Key words: Glycine max, PIN-Like (PILS) gene family, nodule, symbiotic nitrogen fixation

Table 1

Basic information of GmPILS gene family"

基因名称
Gene name		 基因ID
Gene ID		 氨基酸数量
No. of amino acids		 内含子数量
No. of introns		 5'-3'坐标
5'-3' corrdinates
GmPILS1a Glyma.10G189100 313 6 Chr10: 42227422-42231792
GmPILS1b Glyma.20G201600 400 10 Chr20: 43857079-43862374
GmPILS1c Glyma.10G189000 400 10 Chr10: 42220046-42225237
GmPILS1d Glyma.20G201700 259 8 Chr20: 43863679-43868413
GmPILS1e Glyma.07G113100 418 9 Chr07: 11724201-11741130
GmPILS1f Glyma.07G113200 418 11 Chr07: 11780634-11792223
GmPILS1g Glyma.03G113600 424 10 Chr03: 32066847-32080424
GmPILS1h Glyma.16G114900 297 6 Chr16: 25456379-25485759
GmPILS1i Glyma.11G088600 415 10 Chr11: 6695030-6700783
GmPILS1j Glyma.01G156200 415 9 Chr01: 49361352-49366442
GmPILS1k Glyma.09G195600 414 10 Chr09: 42022526-42029030
GmPILS1l Glyma.16G115500 414 9 Chr16: 25622503-25630816
GmPILS2a Glyma.09G116100 440 1 Chr09: 26549730-26551878
GmPILS2b Glyma.19G072900 445 1 Chr19: 26101897-26103958
GmPILS5a Glyma.11G087300 419 10 Chr11: 6547702-6555660
GmPILS5b Glyma.01G157700 419 10 Chr01: 49570825-49577993
GmPILS5c Glyma.09G196900 409 9 Chr09: 42160775-42168544
GmPILS6a Glyma.09G271100 414 10 Chr09: 48791789-48796501
GmPILS6b Glyma.18G218300 414 10 Chr18: 50525980-50531206

Fig. 1

Gene structures of GmPILS gene family The yellow boxes represent the exons and black lines represent the introns of different GmPILS genes."

Fig. 2

Distribution of GmPILS genes on soybean chromosomes"

Fig. 3

Phylogenetic tree of GmPILS, AtPILS, and OsPILS proteins"

Fig. 4

Relative expression pattern of GmPILSs genes A: the heat map of tissue expression pattern of GmPILS genes, and FPKM is obtained from Phytozome database. B: GmPILS1e, GmPILS1f, GmPILS1i, GmPILS1j, and GmPILS5a gene tissue expression pattern in heat map; GmPILSs expression data comes from qPCP results. Colors in square represent the expression levels of GmPILSs."

Fig. 5

Histochemical localization of GmPILS1e, GmPILS1f, GmPILS1i, GmPILS1j, and GmPILS5a in nodule The figures from left to right are referred to the initiation, expansion, and maturity stages of nodules development. Bar: 200 µm."

Fig. 6

Subcellular localization of GmPILS1e and GmPILS1f A-D: tobacco leaves were used for co-transformation of the mixed bacterial broth of pro35S:GFP-GmPILS (green) or pro35S:GmPILS-GFP (green) and pro35S:HDEL-Tdtoamto (red, as an endoplasmic reticulum localization marker). The co-localization signal profile chart is generated based on the white slash. Bar: 10 μm."

Fig. 7

GmPILS1e and GmPILS1f were involved in the regulation of nitrogenase activity in soybean nodules A-G: phenotype analysis was performed on soybean complex plants after inoculation of rhizobia for 21 days. A: mock, GmPILS1e 1f-RNAi#1 and GmPILS1e 1f-RNAi#2 nodules by semi-crosscutting, bar: 200 µm. B: RT-qPCR analysis of GmPILS1e or GmPILS1f in mock, GmPILS1e 1f-RNAi#1 and GmPILS1e 1f-RNAi#2 nodules, with GmELF1b gene as the internal reference gene. C, D: test the nitrogenase activity of mock, GmPILS1e 1f-RNAi#1 and GmPILS1e 1f-RNAi#2 nodules of the same weight. E: statistic mock, GmPILS1e 1f-RNAi#1 and GmPILS1e 1f-RNAi#2. F: RT-qPCR analysis of GmPILS1f in Mock and 35S::GmPILS1f nodules, with GmELF1b gene as the internal reference gene. G: test the nitrogenase activity of mock and 35S::GmPILS1f nodules. *, **, and *** mean significant difference at the 0.05, 0.01, 0.001 probability levels, respectively. ns: no significant difference."

[1] Sauer M, Kleine-Vehn J. PIN-FORMED and PIN-LIKES auxin transport facilitators. Development, 2019, 146: dev168088.
[2] Friml J, Palme K. Polar auxin transport—old questions and new concepts? Plant Mol Biol, 2002,49:273-284.
[3] Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 2003,115:591-602.
[4] Bohn-Courseau I. Auxin: a major regulator of organogenesis. C R Biol, 2010,333:290-296.
[5] Overvoorde P, Fukaki H, Beeckman T. Auxin control of root development. Cold Spring Harb Perspect Biol, 2010,2:a001537.
[6] Olatunji D, Geelen D, Verstraeten I. Control of endogenous auxin levels in plant root development. Int J Mol Sci, 2017,18:2587.
[7] Korasick D A, Enders T A, Strader L C. Auxin biosynthesis and storage forms. J Exp Bot, 2013,64:2541-2555.
[8] Band L R, Wells D M, Fozard J A, Ghetiu T, French A P, Pound M P, Wilson M H, Yu L, Li W, Hijazi H I, Oh J, Pearce S P, Perez-Amador M A, Yun J, Kramer E, Alonso J M, Godin C, Vernoux T, Hodgman T C, Pridmore T P, Swarup R, King J R, Bennett M J. Systems analysis of auxin transport in the Arabidopsis root apex. Plant Cell, 2014,26:862-875.
[9] Strader L C, Zhao Y. Auxin perception and downstream events. Curr Opin Plant Biol, 2016,33:8-14.
[10] Du Y, Scheres B. Lateral root formation and the multiple roles of auxin. J Exp Bot, 2018,69:155-167.
[11] Lareen A, Burton F, Schäfer P. Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol, 2016,90:575-587.
[12] Lagunas B, Schäfer P, Gifford M L. Housing helpful invaders: the evolutionary and molecular architecture underlying plant root-mutualist microbe interactions. J Exp Bot, 2015,66:2177-2186.
[13] Nishida H, Suzaki T. Nitrate-mediated control of root nodule symbiosis. Curr Opin Plant Biol, 2018,44:129-136.
[14] Oldroyd G E, Murray J D, Poole P S, Downie J A. The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet, 2011,45:119-144.
[15] Suzaki T, Yoro E, Kawaguchi M. Leguminous plants: inventors of root nodules to accommodate symbiotic bacteria. Int Rev Cell Mol Biol, 2015,316:111-158.
[16] Salvagiotti F, Cassman K G, Specht J E, Walters D T, Weiss A, Dobermann A. Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crops Res, 2008,108:1-13.
[17] Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore K S, Wen J, Oldroyd G E, Downie J A, Murray J D. The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell, 2014,26:4680-4701.
[18] Van Noorden G E, Kerim T, Goffard N, Wiblin R, Pellerone F I, Rolfe B G, Mathesius U. Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol, 2007,144:1115-1131.
[19] Takanashi K, Sugiyama A, Yazaki K. Involvement of auxin distribution in root nodule development of Lotus japonicus. Planta, 2011,234:73-81.
[20] Suzaki T, Yano K, Ito M, Umehara Y, Suganuma N, Kawaguchi M. Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development, 2012,139:3997-4006.
[21] Hirsch A M, Bhuvaneswari T V, Torrey J G, Bisseling T. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA, 1989,86:1244-1248.
[22] Rightmyer A P, Long S R. Pseudonodule formation by wild-type and symbiotic mutant Medicago truncatula in response to auxin transport inhibitors. Mol Plant Microbe Interact, 2011,24:1372-1384.
[23] Wang Y, Yang W, Zuo Y, Zhu L, Hastwell A H, Chen L, Tian Y, Su C, Ferguson B J, Li X. GmYUC2a mediates auxin biosynthesis during root development and nodulation in soybean. J Exp Bot, 2019,70:3165-3176.
[24] Roy S, Robson F, Lilley J, Liu C W, Cheng X, Wen J, Walker S, Sun J, Cousins D, Bone C, Bennett M J, Downie J A, Swarup R, Oldroyd G, Murray J D. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis. Plant Physiol, 2017,174:326-338.
[25] Kohlen W, Ng J L P, Deinum E E, Mathesius U. Auxin transport, metabolism, and signalling during nodule initiation: indeterminate and determinate nodules. J Exp Bot, 2018,69:229-244.
[26] Liu H, Zhang C, Yang J, Yu N, Wang E. Hormone modulation of legume-rhizobial symbiosis. J Integr Plant Biol, 2018,60:632-648.
[27] Heckmann A B, Sandal N, Bek A S, Madsen L H, Jurkiewicz A, Nielsen M W, Tirichine L, Stougaard J. Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol Plant Microbe Interact, 2011,24:1385-1395.
[28] Peláez-Vico M A, Bernabéu-Roda L, Kohlen W, Soto M J, López-Ráez J A. Strigolactones in the Rhizobium-legume symbiosis: stimulatory effect on bacterial surface motility and down-regulation of their levels in nodulated plants. Plant Sci, 2016,245:119-127.
[29] Buhian W P, Bensmihen S. Mini-review: nod factor regulation of phytohormone signaling and homeostasis during rhizobia-legume symbiosis. Front Plant Sci, 2018,9:1247.
[30] Ferguson B J, Mathesius U. Phytohormone regulation of legume-rhizobia interactions. J Chem Ecol, 2014,40:770-790.
[31] Friml J. Auxin transport—shaping the plant. Curr Opin Plant Biol, 2003,6:7-12.
[32] Barbez E, Kubes M, Rolcik J, Beziat C, Pencik A, Wang B, Rosquete M R, Zhu J, Dobrev P I, Lee Y, Zazimalova E, Petrasek J, Geisler M, Friml J, Kleine-Vehn J. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature, 2012,485:119-122.
[33] Feraru E, Feraru M I, Barbez E, Waidmann S, Sun L, Gaidora A, Kleine-Vehn J. PILS6 is a temperature-sensitive regulator of nuclear auxin input and organ growth in Arabidopsis thaliana. Proc Natl Acad Sci USA, 2019,116:3893-3898.
[34] Beziat C, Barbez E, Feraru M I, Lucyshyn D, Kleine-Vehn J. Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition. Nat Plants, 2017,3:17105.
[35] Feraru E, Vosolsobe S, Feraru M I, Petrasek J, Kleine-Vehn J. Evolution and structural diversification of PILS putative auxin carriers in plants. Front Plant Sci, 2012,3:227.
[36] 叶梅霞, 刘军梅, 李昊, 崔东清, 王静澄, 张志毅, 安新民. amiRNAi-实现高效稳定的特异基因沉默新方法. 中国生物工程杂志, 2010,30(8):118-125.
Ye M X, Liu J M, Li H, Cui D Q, Wang J C, Zhang Z Y, An X M,. amiRNAi: a new approach for highly specific and stable gene silencing. China Biotechnol, 2010,30(8):118-25 (in Chinese with English abstract).
[37] Kereszt A, Li D, Indrasumunar A, Nguyen C D, Nontachaiyapoom S, Kinkema M, Gresshoff P M. Agrobacterium rhizogenes- mediated transformation of soybean to study root biology. Nat Protoc, 2007,2:948-952.
[38] Huang D, Sun Y, Ma Z, Ke M, Cui Y, Chen Z, Chen C, Ji C, Tran T M, Yang L, Lam S M, Han Y, Shu G, Friml J, Miao Y, Jiang L, Chen X. Salicylic acid-mediated plasmodesmal closure via remorin-dependent lipid organization. Proc Natl Acad Sci USA, 2019,116:21274-21284.
[39] David K A, Apte S K, Banerji A, Thomas J. Acetylene reduction assay for nitrogenase activity: gas chromatographic determination of ethylene per sample in less than one minute. Appl Environ Microbiol, 1980,39:1078-1080.
[40] Li X, Zheng J, Yang Y, Liao H. INCREASING NODULE SIZE1 expression is required for normal rhizobial symbiosis and nodule development. Plant Physiol, 2018,178:1233-1248.
[41] 王益军, 吕燕萍, 谢秦, 邓德祥, 卞云龙. 高粱全基因组生长素原初响应基因Aux/IAA的序列特征分析. 作物学报, 2010,36:688-694.
Wang Y J, Lyu Y P, Xie Q, Deng D X, Bian Y L. Whole-genome sequence characterization of primary auxin-responsive Aux/IAA gene family in Sorghum (Sorghum bicolor L.). Acta Agron Sin, 2010,36:688-694 (in Chinese with English abstract).
[42] Dubrovsky J G, Sauer M, Napsucialy-Mendivil S, Ivanchenko M G, Friml J, Shishkova S, Celenza J, Benková E. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA, 2008,105:8790-8794.
[43] Krupinski P, Jönsson H. Modeling auxin-regulated development. Cold Spring Harb Perspect Biol, 2010,2:a001560.
[44] Mohanta T K, Mohanta N, Bae H. Identification and expression analysis of PIN-Like (PILS) gene family of rice treated with auxin and cytokinin. Genes (Basel), 2015,6:622-640.
[45] Laxmi A, Pan J, Morsy M, Chen R. Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS One, 2008,3:e1510.
[46] Halliday K J, Martínez-García J F, Josse E M. Integration of light and auxin signaling. Cold Spring Harb Perspect Biol, 2009,1:a001586.
[47] Leyser O. Dynamic integration of auxin transport and signalling. Curr Biol, 2006,16:R424-433.
[48] Muday G K, Murphy A S. An emerging model of auxin transport regulation. Plant Cell, 2002,14:293-299.
[49] Zazímalová E, Murphy A S, Yang H, Hoyerová K, Hosek P. Auxin transporters—why so many? Cold Spring Harb Perspect Biol, 2010,2:a001552.
[50] Petrásek J, Friml J. Auxin transport routes in plant development. Development, 2009,136:2675-2688.
[51] Alemneh A A, Zhou Y, Ryder M H, Denton M D. Mechanisms in plant growth-promoting rhizobacteria that enhance legume- rhizobial symbioses. J Appl Microbiol, 2020,129:1133-1156.
[52] Hasan S A, Hayat S, Ali B, Ahmad A. A comparative effect of IAA and 4-Cl-IAA on growth, nodulation and nitrogen fixation in Vigna radiate(L.) Wilczek. Acta Physiol Plant, 2008,30:35-41.
[53] Kaneshiro T, Kwolek W F. Stimulated nodulation of soybeans by Rhizobium japonicum mutant (B-14075) that catabolizes the conversion of tryptophan to indol-3yl-acetic acid. Plant Sci, 1985,42:141-146.
[54] Eli Y, Yaacov O, Amos D. Possible mode of action of Azospirillum brasilense strain Cd on the root morphology and nodule formation in burr medic(Medicago polymorpha). Can J Microbiol, 1990,36:10-14.
[55] Chakrabarti J, Chatterjee S, Ghosh S, Chatterjee N C, Dutta S. Synergism of VAM and Rhizobium on production and metabolism of IAA in roots and root nodules of Vigna mungo. Curr Microbiol, 2010,61:203-209.
[56] Ghosh P K, Saha P, Mayilraj S, Maiti T K. Role of IAA metabolizing enzymes on production of IAA in root, nodule of Cajanus cajan and its PGP Rhizobium sp. Biocatal Agric Biotechnol, 2013,2:234-239.
[57] Hunter W J. Influence of 5-methyltryptophan-resistant Bradyrhizobium japonicum on soybean root nodule indole-3-acetic acid content. Appl Environ Microbiol, 1987,53:1051-1055.
[58] Kretovich V L, Alekseeva I I, Tsivina N Z. Content of beta-indolylacetic in root nodules and roots of lupine. Sov Plant Physiol, 1972,19:421-424.
[59] Hunter W J. Indole-3-acetic acid production by bacteroids from soybean root nodules. Physiol Plant, 2010,76:31-36.
[60] Defez R, Andreozzi A, Dickinson M, Charlton A, Tadini L, Pesaresi P, Bianco C. Improved drought stress response in alfalfa plants nodulated by an IAA over-producing Rhizobium strain. Front Microbiol, 2017,8:2466.
[61] Defez R, Andreozzi A, Romano S, Pocsfalvi G, Fiume I, Esposito R, Angelini C, Bianco C. Bacterial IAA-delivery into Medicago root nodules triggers a balanced stimulation of C and N metabolism leading to a biomass increase. Microorganisms, 2019,7:403.
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