Exogenous strigolactones promote lateral root growth by reducing the endogenous auxin level in rapeseed
MA Ni, WAN Lin, ZHAO Wei, LIU Hong-fang, LI Jun, ZHANG Chun-lei
Oil Crops Research Institute, Chinese Academy of Agricultural Sciences/Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs/Key Laboratory of Crop Physiology and Production, Ministry of Agriculture and Rural Affairs, Wuhan 430062, P.R.China
Strigolactones (SLs) are newly discovered plant hormones which regulate the normal development of different plant organs, especially root architecture. Lateral root formation of rapeseed seedlings before winter has great effects on the plant growth and seed yield. Here, we treated the seedlings of Zhongshuang 11 (ZS11), an elite conventional rapeseed cultivar, with different concentrations of GR24 (a synthetic analogue of strigolactones), and found that a low concentration (0.18 µmol L–1) of GR24 could significantly increase the lateral root growth, shoot growth, and root/shoot ratio of seedlings. RNA-Seq analysis of lateral roots at 12 h, 1 d, 4 d, and 7 d after GR24 treatment showed that 2 301, 4 626, 1 595, and 783 genes were significantly differentially expressed, respectively. Function enrichment analysis revealed that the plant hormone transduction pathway, tryptophan metabolism, and the phenylpropanoid biosynthesis pathway were over-represented. Moreover, transcription factors, including AP2/ERF, AUX/IAA, NAC, MYB, and WRKY, were up-regulated at 1 d after GR24 treatment. Metabolomics profiling further demonstrated that the amounts of various metabolites, such as indole-3-acetic acid (IAA) and cis-zeatin were drastically altered. In particular, the concentrations of endogenous IAA significantly decreased by 52.4 and 75.8% at 12 h and 1 d after GR24 treatment, respectively. Our study indicated that low concentrations of exogenous SLs could promote the lateral root growth of rapeseed through interaction with other phytohormones, which provides useful clues for the effects of SLs on root architecture and crop productivity.
Received: 08 October 2018
|Fund: Funds were provided by the National Key Research and Development Program of China (2018YFD1000900).
Correspondence MA Ni, E-mail: email@example.com; ZHANG Chun-lei, Tel: +86-27-86739796, Fax: +86-27-86816451, E-mail: firstname.lastname@example.org
Cite this article:
MA Ni, WAN Lin, ZHAO Wei, LIU Hong-fang, LI Jun, ZHANG Chun-lei.
Exogenous strigolactones promote lateral root growth by reducing the endogenous auxin level in rapeseed. Journal of Integrative Agriculture, 19(2): 465-482.
| Beemster G T, Baskin T I. 1998. Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiology, 116, 1515–1526.
Berriri S, Garcia A V, Dit Frey N F, Rozhon W, Pateyron S, Leonhardt N, Montillet J L, Leung J, Hirt H, Colcombet J. 2012. Constitutively active mitogen-activated protein kinase versions reveal functions of Arabidopsis MPK4 in pathogen defense signaling. The Plant Cell, 24, 4281–4293.
Bolger A M, Lohse M, Usadel B. 2014. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.
Brewer P B, Koltai H, Beveridge C A. 2013. Diverse roles of strigolactones in plant development. Molecular Plant, 6, 18–28.
Chalhoub B, Denoeud F, Liu S, Parkin I A, Tang H, Wang X, Chiquet J, Belcram H, Tong C B, Samans B, Corréa M, Silva C D, Just J, Falentin C, Koh C S, Clainche I L, Bernard M, Bento P, Noel B, Labadie K, et?al. 2014. Early allopolyploid evolution in the post - Neolithic Brassica napus oilseed genome. Science, 345, 950–953.
Chen W, Gong L, Guo Z, Wang W S, Zhang H Y, Liu X Q, Yu S B, Xiong L Z, 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, Ruyter-Spira C, Bouwmeester H. 2013. The interaction between strigolactones and other plant hormones in the regulation of plant development. Frontiers in Plant Science, 4, 1–16.
Cho H, Ryu H, Rho S, Hill K, Smith S, Audenaert D, Park J, Han S, Beeckman T, Bennett M, Hwang D, Smet I, Hwang I. 2014. A secreted peptideacts on BIN2-mediated phosphorylation of ARFs to potentiate auxin responseduring lateral root development. Nature Cell Biology, 16, 66–76.
Dalal M, Sahu S, Tiwari S, Rao A R, Gaikwad K. 2018. Transcriptome analysis reveals interplay between hormones, ROS metabolism and cell wall biosynthesis for drought-induced root growth in wheat. Plant Physiology and Biochemistry, 130, 482–492.
Diepenbrock W. 2000. Yield analysis of winter oilseed rape (Brassica napus L.): A review. Field Crops Research, 67, 35–49.
Du Y J, Scheres B. 2018. Lateral root formation and the multiple roles of auxin. Journal of Experimental Botany, 69, 155–167.
Dun E A, Germain A S, Rameau C, Beveridge C A. 2012. Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiology, 158, 487–498.
Dunand C, Crevecoeur M, Penel C. 2007. Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: Possible interaction with peroxidases. New Phytologist, 174, 332–341.
Escobar-Sepúlveda H F, Trejo-Téllez L I, García-Morales S, Gómez-Merino F C. 2017. Expression patterns and promoter analyses of aluminum-responsive NAC genes suggest a possible growth regulation of rice mediated by aluminum, hormones and NAC transcription factors. PLoS ONE, 12, e0186084.
Fang S Q, Clark R T, Zheng Y, Iyer-Pascuzzi A S, Weitz J S, Kochian L V, Edelsbrunner H, Liao H, Benfey P N. 2013. Genotypic recognition and spatial responses by rice roots. Proceeding of the National Academy of Sciences of the United States of America, 110, 2670–2675.
Foo E, Reid J B. 2013. Strigolactones: New physiological roles for an ancient signal. Journal of Plant Growth Regulation, 32, 429–442.
Fukaki H, Tasaka M. 2009. Hormone interactions during lateral root formation. Plant Molecular Biology, 69, 437–449.
Gao F, Yao H, Zhao H, Zhou J, Luo X, Huang Y, Li C, Chen H, Wu Q. 2016. Tartary buckwheat FtMYB10 encodes an R2R3-MYB transcription factor that acts as a novel negative regulator of salt and drought response in transgenic Arabidopsis. Plant Physiology and Biochemistry, 109, 387–396.
Hao Y J, Wei W, Song Q X, Chen H W, Zhang Y Q, Wang F, Zou H F, Lei G, Tian A G, Zhang W K, Ma B, Zhang J S, Chen S Y. 2011. Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. The Plant Journal, 68, 302–313.
Ivanchenko M G, Muday G K, Dubrovsky J G. 2008. Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis Thaliana. The Plant Journal, 55, 335–347.
Ivanchenko M G, Napsucialy-Mendivil S, Dubrovsky J G. 2010. Auxin-induced inhibition of lateral root initiation contributes to root system shaping in Arabidopsis thaliana. The Plant Journal, 64, 740–752.
Jin J H, Wang M, Zhang H X, Khan A, Wei A M, Luo D X, Gong Z H. 2018. Genome-wide identification of the AP2/ERF transcription factor family in pepper (Capsicum annuum L.). Genome, 61, 663-674.
Kapulnik Y, Delaux P M, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier J P, Bécard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H. 2011. Strigolactones affect lateral root formation and root hair elongation in Arabidopsis. Planta, 233, 209–216.
Kapulnik Y, Koltai H. 2014. Strigolactone involvement in root development, response to abiotic stress, and interactions with the biotic soil environment. Plant Physiology, 166, 560–569.
Khosla A, Nelson D C. 2016. Strigolactones, super hormones in the fight against striga. Current Opinion in Plant Biology, 33, 57–63.
Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12, 357.
Koltai H. 2011a. Strigolactones ability to regulate root development may be executed by induction of the ethylene pathway. Plant Signaling & Behavior, 6, 1004–1005.
Koltai H. 2011b. Strigolactones are regulators of root development. New Phytologist, 190, 545–549.
Koltai H. 2014. Implications of non-specific strigolactone signaling in the rhizosphere. Plant Science, 225, 9–14.
Koltai H, Dor E, Hershenhorn J, Joel D M, Weininger S, Lekalla S, Shealtiel H, Chaitali B, Eliahu E, Resnick N, Barg R, Kapulnik Y. 2010. Strigolactones’ effect on root growth and root hair elongation may be mediated by auxin efflux carriers. Journal of Plant Growth Regulation, 29, 129–136.
Kurepa J, Shull T E, Karunadasa S S, Smalle J A. 2018. Modulation of auxin and cytokinin responses by early steps of the phenylpropanoid pathway. BMC Plant Biology, 18, 278.
Lavenus J, Goh T, Robers I, Guyomar?h S, Lucas M, Smet I D, Fukaki H, Beeckman T, Bennett M, Laplaze L. 2013. Lateral root development in Arabidopsis: Fifty shades of auxin. Trends in Plant Sciences, 18, 450–458.
Lewis D R, Negi S, Sukumar P, Muday G K. 2011. Ethylene inhibits lateral root development, increase IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development, 138, 3485–3495.
Li Y H, Wei F, Dong X Y, Peng J H, Liu S Y, Chen H. 2011. Simultaneous analysis of multiple endogenous plant hormones in leaf tissue of oilseed rape by solid-phase extraction coupled with high performance liquid chromatography-electrospray ionization tandem mass spectrometry. Phytochemical Analysis, 22, 442–449.
Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
López-Bucio J, Cruz-Ram??rez A, Herrera-Estrella L. 2003. The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology, 6, 280–287.
Lu C, Napier J A, Clemente T E, Cahoon E B. 2011. New frontiers in oilseed biotechology: Meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications. Current Opinion in Plant Biology, 22, 252–259.
Ma N, Hu C, Wan L, Hu Q, Xiong J L, Zhang C L. 2017. Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L.) by regulating gene expression. Frontiers in Plant Sciences, 8, 1671.
Malamy J E. 2005. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell & Environment, 28, 67–77.
Marhavý P, Vanstraelen M, De Rybel B, Ding Z J, Bennett M J, Beeckman T, Benkov E. 2013. Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO Journal, 32, 149–158.
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti V B, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F. 2011. ROS signaling: The new wave? Trends in Plant Science, 16, 300–309.
Nakano T, Suzuki K, Fujimura T, Shinshi H. 2006. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiology, 140, 411–432.
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2012. NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta, 1819, 97–103.
Negi S, Ivanchenko M G, Muday G K. 2008. Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. The Plant Journal, 55, 175–187.
Negi S, Sukumar P, Liu X, Cohen J D, Muday G K. 2010. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. The Plant Journal, 61, 3–15.
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. 2007. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. The Plant Cell, 19, 118–130.
Opitz N, Marcon C, Paschold A, Malik W A, Lithio A, Brandt R, Piepho H P, Nettleton D, Hochholdinger F. 2015. Extensive tissue-specific transcriptomic plasticity in maize primary roots upon water deficit. Journal of Experimental Botany, 67, 1095–1107.
Péret B, Middleton A M, French A P, Larrieu A, Bishopp A, Njo M, Wells D M, Porco S, Mellor N, Band L R, Casimiro I, Kleine-Vehn J, Vanneste S, Sairanen I, Mallet R, Sandberg G, Ljung K, Beeckman T, Benkova E, Friml J, et?al. 2013. Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Molecular Systems Biology, 9, 699.
Porco S, Larrieu A, Du Y, Gaudinier A, Goh T, Swarup K, Swarup R, Kuempers B, Bishopp A, Lavenus J, Casimiro I, Hill K I, Benkova E, Fukaki H, Brady S M, Scheres B, Péret B, Bennett M J. 2016. Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3. Development, 143, 3340–3349.
Raja V, Majeed U, Kang H, Andrabi K I, John R. 2017. Abiotic stress: Interplay between ROS, hormones and MAPKs. Environmental and Experimental Botany, 137, 142–157.
Ruyter-Spira C, Kohlen W, Charnikhova T, Van Zeijl A, Van Bezouwen L, De Ruijter N, Cardoso C, Lopez-Raez J A, Matusova R, Bours R, Verstappen F, Bouwmeester H. 2011. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another belowground role for strigolactones? Plant Physiology, 155, 721–734.
Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E. 2007. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. The Plant Cell, 19, 2197–2212.
Saini S, Sharma I, Kaur N, Pati P K. 2013. Auxin: A master regulator in plant root development. Plant Cell Report, 32, 741–757.
Seo P J, Park C M. 2009. Auxin homeostasis during lateral root development under drought condition. Plant Signal Behavior, 4, 1002–1004.
Shinohara N, Taylor C, Leyser O. 2013. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biology, 11, e1001474.
Stepanova A N, Robertson-Hoyt J, Yun J, Benavente L M, Xie D Y, Dolezal K, Schlereth A, Jürgens G, Alonso J M. 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell, 133, 177–191.
Stepanova A N, Yun J, Likhacheva A V, Alonso J M. 2007. Multilevel interactions between ethylene and auxin in Arabidopsis roots. The Plant Cell, 19, 2169–2185.
Strzalka W, Ziemienowicz A. 2011. Proliferating cell nuclear antigen (PCNA): A key factor in DNA replication and cell cycle regulation. Annals of Botany, 107, 1127–1140.
Sun H, Tao J, Hou M, Huang S, Chen S, Liang Z, Xie T, Wei Y, Xie X, Yoneyama K, Xu G, Zhang Y. 2015. A strigolactone signal is required for root formation in rice. Annals of Botany, 115, 1155–1162.
Sun P, Tian Q Y, Chen J, Zhang W H. 2010. Aluminium-induced inhibition of root elongation in Arabidopsisis mediated by ethylene and auxin. Journal of Experimental Botany, 61, 347–356.
Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster G T, Sandberg G, Bhalerao R, Ljung K, Bennett M J. 2007. Ethylene up regulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. The Plant Cell, 19, 2186–2196.
Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki M K, Harper R M, Liscum E, Yamamoto K T. 2004. MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. The Plant Cell, 16, 379–393.
Trupiano D, Yordanov Y, Regan S, Meilan R, Tschaplinski T, Gabriella S S, Busov V. 2013. Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus. Planta, 238, 271–282.
Wen W W, Li D, Li X, Gao X Q, Li W Q, Li H H, Liu J, Liu H J, Chen W, Luo J, Yan J B. 2014. Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nature Communications, 5, 3438.
Xu J, Zhang S Q. 2015. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends of Plant Science, 20, 56–64.
Xu Y Y, Li X G, Lin J, Wang Z H, Yang Q S, Chang Y H. 2015. Transcriptome sequencing and analysis of major genes involved in calcium signaling pathways in pear plants (Pyrus calleryana Decne.). BMC Genomics, 16, 738.
Yang H L, Liu J, Huang S M, Guo T T, Deng L B, Hua W. 2014. Selection and evaluation of novel reference genes for quantitative reverse transcription PCR (qRT-PCR) based on genome and transcriptome data in Brassica napus L. Gene, 538, 113–122.
Yoneyama K, Xie X N, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K. 2008. Strigolactones, host recognition signals for root parasitic plants and Arbuscular mycorrhizal fungi, from fabaceae plants. New Phytologist, 179, 484–494.
Zhang N, Zhang H J, Zhao B, Sun Q Q, Cao Y Y, Li R, Wu X X, Weeda S, Li L, Ren S, Reiter R J, Guo Y D. 2014. The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation. Journal of Pineal Research, 56, 39–50.
Zheng Y, Jiao C, Sun H, Rosli H G, Pombo M A, Zhang P, Banf M, Dai X, Martin G B, Giovannoni J J. 2016. iTAK: A program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Molecular Plant, 9, 1667–1670.
Zwanenburg B, Pospíšil T, Zeljkovi? S C. 2016. Strigolactones: New plant hormones in action. Planta, 243, 1311–1326.
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