Abstract
RNA-Seq (RNA-Sequencing) allows for precise quantitative determination of global gene expression patterns and has therefore revolutionized transcriptome analyses in maize. In recent years, genetic analyses have identified numerous genes that control maize root system architecture and root hair elongation. In addition, RNA-Seq has been applied to dissect structure and function of individual roots. In this chapter, we summarize the current state of the transcriptomic dissection of maize root development on the level of whole roots, tissues, and individual cells. Moreover, we highlight the current knowledge of transcriptome responses of maize roots to drought stress and nutrient availability. Finally, we outline novel findings related to gene expression plasticity in primary roots of maize hybrids during the early manifestation of heterosis.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Babé A, Lavigne T, Severin J-P, Nagel KA, Walter A, Chaumont F, Batoko H, Beeckman T, Draye X (2012) Repression of early lateral root initiation events by transient water deficit in barley and maize. Philos Trans R Soc B Biol Sci 367:1534–1541
Baldauf JA, Marcon C, Lithio A, Vedder L, Altrogge L, Piepho H-P, Schoof H, Nettleton D, Hochholdinger F (2018) Single-parent expression is a general mechanism driving extensive complementation of non-syntenic genes in maize hybrids. Curr Biol 28:431–437
Baldauf JA, Marcon C, Paschold A, Hochholdinger F (2016) Nonsyntenic genes drive tissue-specific dynamics of differential, nonadditive and allelic expression patterns in maize hybrids. Plant Physiol 171:1144–1155
Bao Y, Aggarwal P, Robbins NE, Sturrock CJ, Thompson MC, Tan HQ, Tham C, Duan L, Rodriguez PL, Vernoux T et al (2014) Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc Natl Acad Sci 111:9319–9324
Burton AL, Brown KM, Lynch JP (2013) Phenotypic diversity of root anatomical and architectural traits in Zea species. Crop Sci 53:1042–1055
Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk LA, Lamkemeyer T, Fladerer C, Madlung J, Barbazuk B et al (2007) Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol 145: 575–588
Forde BG (2014) Nitrogen signalling pathways shaping root system architecture: an update. Curr Opin Plant Biol 21:30–36
Gao Y, Lynch JP (2016) Reduced crown root number improves water acquisition under water deficit stress in maize (Zea mays L.). J Exp Bot 67:4545–4557
Gaudin ACM, Mcclymont SA, Holmes BM, Lyons E, Raizada MN (2011) Novel temporal, fine-scale and growth variation phenotypes in roots of adult-stage maize (Zea mays L.) in response to low nitrogen stress. Plant Cell Environ 34:2122–2137
Giehl RFH, von Wiren N (2014) Root nutrient foraging. Plant Physiol 166:509–517
Guo Y, Chen F, Zhang F, Mi G (2005) Auxin transport from shoot to root is involved in the response of lateral root growth to localized supply of nitrate in maize. Plant Sci 169:894–900
He X, Qu B, Li W, Zhao X, Teng W, Ma W, Ren Y, Li B, Li Z, Tong Y (2015) The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiol 169:1991–2005
Hetz W, Hochholdinger F, Schwall M, Feix G (1996) Isolation and characterization of rtcs, a maize mutant deficient in the formation of nodal roots. Plant J 10:845–857
Hey S, Baldauf JA, Opitz N, Lithio A, Pasha A, Provart N, Nettleton D, Hochholdinger F (2017) Complexity and specificity of the maize (Zea mays L.) root hair transcriptome. J Exp Bot 68:2175–2185
Hochholdinger F (2009) The maize root system: morphology, anatomy, and genetics. In: Bennetzen JL, Hake SC (eds) Handb. Maize, Springer, pp 145–160
Hochholdinger F, Feix G (1998) Early post-embryonic root formation is specifically affected in the maize mutant lrt1. Plant J 16:247–255
Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432
Hochholdinger F, Marcon C, Baldauf JA, Frey F, Yu P (2018b) Proteomics of maize root development. Front Plant Sci 9:143
Hochholdinger F, Park WJ, Sauer M, Woll K (2004a) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci 9:42–48
Hochholdinger F, Woll K, Sauer M, Dembinsky D (2004b) Genetic dissection of root formation in maize (Zea mays) reveals root type specific developmental programmes. Ann Bot 93:359–368
Hochholdinger F, Yu P, Marcon C (2018a) Genetic control of root system development in maize. Trends Plant Sci 23:79–88
Hoecker N, Keller B, Muthreich N (2008) Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends. Genetics 179:1275–1283
Hoecker N, Keller B, Piepho HP, Hochholdinger F (2006) Manifestation of heterosis during early maize (Zea mays L.) root development. Theor Appl Genet 112:421–429
Ishikawa H, Evans ML (1995) Specialized zones of development in roots. Plant Physiol 109:725–727
Jansen L, Hollunder J, Roberts I, Forestan C, Fonteyne P, Van Quickenborne C, Zhen RG, Mckersie B, Parizot B, Beeckman T (2013) Comparative transcriptomics as a tool for the identification of root branching genes in maize. Plant Biotechnol J 11:1092–1102
Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei X, Chin C et al (2017) Improved maize reference genome with single-molecule technologies. Nature 546:524–527
Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics 2:466–479
Liu J, An X, Cheng L, Chen F, Bao J, Yuan L, Zhang F, Mi G (2010) Auxin transport in maize roots in response to localized nitrate supply. Ann Bot 106:1019–1026
Ludwig Y, Hochholdinger F (2014) Laser microdissection of plant cells. In: Žárský V, Cvrčková F (eds) Plant cell morphogenesis. Methods in molecular biology. Humana Press, Totowa, pp 249–258
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049
Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112:347–357
Manoli A, Begheldo M, Genre A, Lanfranco L, Trevisan S, Quaggiotti S (2014) NO homeostasis is a key regulator of early nitrate perception and root elongation in maize. J Exp Bot 65:185–200
Marcon C, Paschold A, Malik WA, Lithio A, Baldauf JA, Altrogge L, Opitz N, Lanz C, Schoof H, Nettleton D et al (2017) Stability of single parent gene expression complementation in maize hybrids upon water deficit stress. Plant Physiol 173:1247–1257
Muthreich N, Majer C, Beatty M, Paschold A, Schutzenmeister A, Fu Y, Malik WA, Schnable PS, Piepho H-P, Sakai H et al (2013) Comparative transcriptome profiling of maize coleoptilar nodes during shoot-borne root initiation. Plant Physiol 163:419–430
Nakazono M, Qiu F, Borsuk LA, Schnable PS (2003) Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15:583–596
Nestler J, Liu S, Wen TJ, Paschold A, Marcon C, Tang HM, Li D, Li L, Meeley RB, Sakai H et al (2014) Roothairless5, which functions in maize (Zea mays L.) root hair initiation and elongation encodes a monocot-specific NADPH oxidase. Plant J 79:729–740
Opitz N, Marcon C, Paschold A, Malik WA, Lithio A, Brandt R, Piepho HP, Nettleton D, Hochholdinger F (2016) Extensive tissue-specific transcriptomic plasticity in maize primary roots upon water deficit. J Exp Bot 67:1095–1107
Opitz N, Paschold A, Marcon C, Malik WA, Lanz C, Piepho H-P, Hochholdinger F (2014) Transcriptomic complexity in young maize primary roots in response to low water potentials. BMC Genom 15:741
Paschold A, Jia Y, Marcon C, Lund S, Larson NB, Yeh C-T, Ossowski S, Lanz C, Nettleton D, Schnable PS et al (2012) Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. Genome Res 22:2445–2454
Paschold A, Larson NB, Marcon C, Schnable JC, Yeh CT, Lanz C, Nettleton D, Piepho H-P, Schnable PS, Hochholdinger F (2014) Nonsyntenic genes drive highly dynamic complementation of gene expression in maize hybrids. Plant Cell 26:3939–3948
Peter R, Eschholz TW, Stamp P, Liedgens M (2009) Early growth of flint maize landraces under cool conditions. Crop Sci 49:169–178
Ribaut JM, Betran J, Monneveux P, Setter T (2009) Drought tolerance in maize. In: Bennetzen JL, Hake SC (eds) Handb. Maize, Springer, pp 311–344
Robbins NE, Dinneny JR (2018) Growth is required for perception of water availability to pattern root branches in plants. Proc Natl Acad Sci 201710709
Rogers ED, Benfey PN (2015) Regulation of plant root system architecture: implications for crop advancement. Curr Opin Biotechnol 32:93–98
Saleem M, Lamkemeyer T, Schützenmeister A, Fladerer C, Piepho HP, Nordheim A, Hochholdinger F (2009) Tissue specific control of the maize (Zea mays L.) embryo, cortical parenchyma, and stele proteomes by RUM1 which regulates seminal and lateral root initiation. J Proteome Res 8:2285–2297
Schnable PS, Springer NM (2013) Progress toward understanding heterosis in crop plants. Annu Rev Plant Biol 64:13.1–13.18
Schnable JC, Springer NM, Freeling M (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Nat Acad Sci 108:4069–4074
Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115
Sebastian J, Yee M-C, Goudinho Viana W, Rellán-Álvarez R, Feldman M, Priest HD, Trontin C, Lee T, Jiang H, Baxter I et al (2016) Grasses suppress shoot-borne roots to conserve water during drought. Proc Natl Acad Sci 113:8861–8866
Stelpflug SC, Rajandeep S, Vaillancourt B, Hirsch CN, Buell CR, De Leon N, Kaeppler SM (2015) An expanded maize gene expression atlas based on RNA-sequencing and its use to explore root development. Plant Genome 9:314–362
Tai H, Lu X, Opitz N, Marcon C, Paschold A, Lithio A, Nettleton D, Hochholdinger F (2016) Transcriptomic and anatomical complexity of primary, seminal, and crown roots highlight root type-specific functional diversity in maize (Zea mays L.). J Exp Bot 67:1123–1135
Tai H, Opitz N, Lithio A, Lu X, Nettleton D, Hochholdinger F (2017) Non-syntenic genes drive RTCS-dependent regulation of the embryo transcriptome during formation of seminal root primordia in maize (Zea mays L.). J Exp Bot 68:403–414
Taramino G, Sauer M, Stauffer JL, Multani D, Niu X, Sakai H, Hochholdinger F (2007) The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation. Plant J 50:649–659
Tian Q, Chen F, Liu J, Zhang F, Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J Plant Physiol 165:942–951
Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2013) Maize root growth angles become steeper under low N conditions. Field Crop Res 140:18–31
Trevisan S, Manoli A, Begheldo M, Nonis A, Enna M, Vaccaro S, Caporale G, Ruperti B, Quaggiotti S (2011) Transcriptome analysis reveals coordinated spatiotemporal regulation of hemoglobin and nitrate reductase in response to nitrate in maize roots. New Phytol 192:338–352
Trevisan S, Manoli A, Ravazzolo L, Botton A, Pivato M, Masi A, Quaggiotti S (2015) Nitrate sensing by the maize root apex transition zone: a merged transcriptomic and proteomic survey. J Exp Bot 66:3699–3715
Wang Y, Mi G, Chen F, Zhang J, Zhang F (2005) Response of root morphology to nitrate supply and its contribution to nitrogen accumulation in maize. J Plant Nutr 27:2189–2202
Woll K, Borsuk L a, Stransky H, Nettleton D, Schnable PS, Hochholdinger F (2005) Isolation, characterization, and pericycle-specific transcriptome analyses of the novel maize lateral and seminal root initiation mutant rum1. Plant Physiol 139:1255–1267
Yu P, Baldauf JA, Lithio A, Marcon C, Nettleton D, Li C, Hochholdinger F (2016) Root type-specific reprogramming of maize pericycle transcriptomes by local high nitrate results in disparate lateral root branching patterns. Plant Physiol 170:1783–1798
Yu P, Eggert K, von Wirén N, Li C, Hochholdinger F (2015) Cell type-specific gene expression analyses by RNA sequencing reveal local high nitrate-triggered lateral root initiation in shoot-borne roots of maize by modulating auxin-related cell cycle regulation. Plant Physiol 169:690–704
Yu P, White PJ, Hochholdinger F, Li C (2014) Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta 240:667–678
Zhang Y, Paschold A, Marcon C, Liu S, Tai H, Nestler J, Yeh C, Opitz N, Lanz C, Schnable PS et al (2014) The Aux/IAA gene rum1 involved in seminal and lateral root formation controls vascular patterning in maize (Zea mays L.) primary roots. J Exp Bot 65:4919–4930
Zhu J, Kaeppler SM, Lynch JP (2005) Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays). Funct Plant Biol 32:749–762
Acknowledgements
Root research in FH’s laboratory supported by the DFG (German Research Foundation) and the BMBF (German Federal Ministry of Education and Research).
Author information
Authors and Affiliations
Contributions
All authors contributed to the writing of this book chapter.
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Yu, P., Marcon, C., Baldauf, J.A., Frey, F., Baer, M., Hochholdinger, F. (2018). Transcriptomic Dissection of Maize Root System Development. In: Bennetzen, J., Flint-Garcia, S., Hirsch, C., Tuberosa, R. (eds) The Maize Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-97427-9_15
Download citation
DOI: https://doi.org/10.1007/978-3-319-97427-9_15
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-97426-2
Online ISBN: 978-3-319-97427-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)