Abstract
Aims
To realize the so-called “Second Green Revolution”, it is imperative to study the roots of crop plants, and identify those traits that improve the efficiency of nitrogen (N) acquisition. We aimed to evaluate how the N acquisition efficiency of six hybrid maize lines commonly grown in northern China depends on their root anatomy.
Methods
Maize hybrids classified as having high nitrogen uptake efficiency (HNUE) and low nitrogen uptake efficiency (LNUE) were grown under high-N and low-N conditions in the greenhouse and the field.
Results
Under N stress in the field and the greenhouse, HNUE increased shoot dry weight, root length density, N content and nitrogen use efficiency compared to LNUE. Low N availability increased the percentage of root cortical aerenchyma and the size of cortical cells. Root anatomy, with greater formation of root cortical aerenchyma and larger cortical cell size, was associated with increased specific nitrogen absorption efficiency (SNAE) and shoot biomass under N stress. Under low N availability, the percentage of aerenchyma and their total area had significant positive correlations with the shoot dry weight, total N uptake, SNAE.
Conclusions
The results suggest that plants in limited N availability form more root cortical aerenchyma and have larger cortical cells, which is of benefit to root growth, soil exploration, N acquisition, and shoot biomass. These observations support the hypothesis that root anatomical phenotypes that affect the metabolic and construction costs of producing root length merit consideration as selection criteria for breeding to improve N acquisition in hybrid maize.
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11 May 2022
A Correction to this paper has been published: https://doi.org/10.1007/s11104-022-05471-9
References
Abiko T, Obara M (2014) Enhancement of porosity and aerenchyma formation in nitrogen-deficient rice roots. Plant Sci 215:76–83. https://doi.org/10.1016/j.plantsci.2013.10.016
Bizimana F, Timilsina A, Dong W, Uwamungu JY, Li XX, Wang YY, Pandey QSP, Hu CS (2021) Effects of long-term nitrogen fertilization on N2O, N2 and their yield-scaled emissions in a temperate semi-arid agro-ecosystem[J]. J Soils Sediments 21(4):1659–1671. https://doi.org/10.1007/s11368-021-02903-4
Burton AL, Williams M, Lynch JP, Brown KM (2012) RootScan: software for high-throughput analysis of root anatomical traits. Plant Soil 357(1):189–203. https://doi.org/10.1007/s11104-012-1138-2
Chen XP, Cui ZL, Vitousek PM, Cassman KG, Matson PA, Bai JS, Meng QF, Hou P, Yue SC, Romheld V, Zhang FS (2011) Integrated soil-crop system management for food security. Proc Natl Acad Sci 108(16):6399–6404. https://doi.org/10.1073/pnas.1101419108
Chimungu JG, Brown KM, Lynch JP (2014a) Large root cortical cell size improves drought tolerance in maize. Plant Physiol 166(4):2166–2178. https://doi.org/10.1104/pp.114.250449
Chimungu JG, Brown KM, Lynch JP (2014b) Reduced root cortical cell file number improves drought tolerance in maize. Plant Physiol 166(4):1943–1955. https://doi.org/10.1104/pp.114.249037
Chimungu JG, Maliro MF, Nalivata PC, Kanyama-Phiri G, Brown KM, Lynch JP (2015) Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.). Field Crops Research 171:86–98. https://doi.org/10.1016/j.fcr.2014.10.009
Clemensson-Lindell A (1994) Triphenyltetrazolium chloride as an indicator of fine-root vitality and environmental stress in coniferous forest stands: applications and limitations. Plant Soil 159(2):297–300. https://doi.org/10.1007/BF00009293
Crist E, Mora C, Engelman R (2017) The interaction of human population, food production, and biodiversity protection. Science 356(6335):260–264. https://doi.org/10.1126/science.aal2011
Galindo-Castañeda T, Brown KM, Lynch JP (2018) Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize. Plant, Cell Environment 41(7):1579–1592. https://doi.org/10.1111/pce.13197
Hirel B, Le GJ, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58(9):2369–2387. https://doi.org/10.1093/jxb/erm097
Huang J, Xu CC, Ridoutt BG, Wang XC, Ren PA (2017) Nitrogen and phosphorus losses and eutrophication potential associated with fertilizer application to cropland in China. J Clean Prod 159:171–179. https://doi.org/10.1016/j.jclepro.2017.05.008
Jaramillo RE, Nord EA, Chimungu JG, Brown KM, Lynch JP (2013) Root cortical burden influences drought tolerance in maize. Ann Bot 112(2):429–437. https://doi.org/10.1093/aob/mct069
Jia XC, Shao LJ, Liu P, Zhao B, Gu LM, Dong ST, Bing SW, Zhang JW, Zhao B (2014) Effect of different nitrogen and irrigation treatments on yield and nitrate leaching of summer maize (Zea mays L.) under lysimeter conditions. Agric Water Manag 137:92–103. https://doi.org/10.1016/j.agwat.2014.02.010
Lambers H, Atkin OK, Millenaar FF (2002) The respiratory patterns in roots in relation to their functioning. In Plant Roots: The Hidden Half (pp. 521–552) Marcel Dekker
Liu Y, Bortier MF, De BHJ, Nijs I (2017) Root distribution responses to three-dimensional soil heterogeneity in experimental mesocosms. Plant Soil 421(1):353–366. https://doi.org/10.1007/s11104-017-3472-x
Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112(2):347–357. https://doi.org/10.1093/aob/mcs293
Lynch JP (2015) Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture. Plant, Cell Environment 38(9):1775–1784. https://doi.org/10.1111/pce.12451
Lynch JP (2019) Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytol 223(2):548–564. https://doi.org/10.1111/nph.15738
Peng Y, Niu J, Peng Z, Zhang F, Li C (2010) Shoot growth potential drives N uptake in maize plants and correlates with root growth in the soil. Field Crop Res 115(1):85–93. https://doi.org/10.1016/j.fcr.2009.10.006
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-roject.org/.
Ramankutty N, Mehrabi Z, Waha K, Jarvis L, Kremen C, Herrero M, Rieseberg LH (2018) Trends in global agricultural land use: implications for environmental health and food security. Annu Rev Plant Biol 69:789–815. https://doi.org/10.1016/j.scitotenv.2015.07.064
Raza S, Miao N, Wang P, Ju X, Chen Z, Zhou J, Kuzyakov Y (2020) Dramatic loss of inorganic carbon by nitrogen-induced soil acidification in Chinese croplands. Glob Change Biol 26(6):3738–3751. https://doi.org/10.1111/gcb.15101
Saengwilai P, Tian X, Lynch JP (2014a) Low crown root number enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiol 166(2):581–589. https://doi.org/10.1104/pp.113.232603
Saengwilai P, Nord EA, Chimungu JG, Brown KM, Lynch JP (2014b) Root cortical aerenchyma enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiol 166(2):726–735. https://doi.org/10.1104/pp.114.241711
Song XT, Liu M, Ju XT, Gao B, Su F, Chen XP, Rees RM (2018) Nitrous oxide emissions increase exponentially when optimum nitrogen fertilizer rates are exceeded in the North China Plain[J]. Environ Sci Technol 52(21):12504–12513. https://doi.org/10.1021/acs.est.8b03931
Sun BR, Gao YZ, Lynch JP (2018) Large crown root number improves topsoil foraging and phosphorus acquisition. Plant Physiol 177(1):90–104. https://doi.org/10.1104/pp.18.00234
Sun Z, Sänger A, Rebensburg P, Lentzsch P, Wirth S, Kaupenjohann M, Meyer-Aurich A (2017) Contrasting effects of biochar on N2O emission and N uptake at different N fertilizer levels on a temperate sandy loam. Sci Total Environ 578:557–565. https://doi.org/10.1016/j.scitotenv.2016.10.230
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. https://doi.org/10.1016/j.fcr.2012.09.010
Wiesmeier M, Hübner R, Kögel-Knabner I (2015) Stagnating crop yields: An overlooked risk for the carbon balance of agricultural soils? Sci Total Environ 536:1045–1051. https://doi.org/10.1016/j.scitotenv.2015.07.064
Xia L, Lam SK, Chen D, Wang J, Tang Q, Yan X (2017) Can knowledge-based N management produce more staple grain with lower greenhouse gas emission and reactive nitrogen pollution? A Meta-Analysis Global Change Biology 23(5):1917–1925. https://doi.org/10.1111/gcb.13455
Yu P, White PJ, Hochholdinger F, Li C (2014) Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta 240(4):667–678. https://doi.org/10.1007/s00425-014-2150-y
Zhan A, Lynch JP (2015) Reduced frequency of lateral root branching improves N capture from low-N soils in maize. J Exp Bot 66(7):2055–2065. https://doi.org/10.1093/jxb/erv007
Zhang DS, Lyu Y, Li HB, Tang XY, Hu R, Rengel Z, Zhang FS, Whalley WR, Davies WJ, Cahill JJF (2020) Neighbouring plants modify maize root foraging for phosphorus: coupling nutrients and neighbours for improved nutrient-use efficiency. New Phytol 226:244–253. https://doi.org/10.1111/nph.16206
Zhu J, Brown KM, Lynch JP (2010) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant, Cell Environment 33(5):740–749. https://doi.org/10.1111/j.1365-3040.2009.02099.x
Acknowledgements
We are grateful for grants from National Natural Science Foundation of China (31771713, 32071959), National Basic Research Program of China (2016YFD0300106), and Shandong Province Key Agricultural Project for Application Technology Innovation (SDAIT02-08).
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Jia, X., Wu, G., Strock, C. et al. Root anatomical phenotypes related to growth under low nitrogen availability in maize (Zea mays L.) hybrids. Plant Soil 474, 265–276 (2022). https://doi.org/10.1007/s11104-022-05331-6
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DOI: https://doi.org/10.1007/s11104-022-05331-6