Abstract
Background and aims
Previous studies showed that the competition-recovery principle is one of the mechanisms underpinning overyielding in wheat/maize intercropping. However, few studies have focused on the effects of root morphological and physiological changes during the recovery growth of late-maturing species. The present study aimed to determine the mechanism underlying the recovery growth in terms of root distribution and nitrogen (N) uptake in response to different N supplies.
Methods
The roots of maize were sampled three times by auger after wheat harvest in the intercropping system with six levels of N application and sole crops at one N-application rate under field condition.
Results
Intercropped maize adjusted its root length density (RLD) and root distribution and enhanced its N absorption per unit root length with increasing soil N concentration. Soil inorganic N concentration had a direct influence on RLD of intercropped maize which was related to shoot N concentration. In addition, maize took up 93% more N per unit root length when intercropped with maize compared with sole cropping.
Conclusions
Our findings show that the recovery growth of late-maturing species involves phenotypic plasticity of maize root architecture, and the enhanced N uptake resulted from extra soil N acquired from the area where wheat was growing before its harvest.
Similar content being viewed by others
References
Aggarwal PK, Garrity DP, Liboon SP, Morris RA (1992) Resource use and plant interactions in a rice-mungbean intercrop. Agron J 84:71–78
Alvarez JM, Vidal EA, Gutiérrez RA (2012) Integration of local and systemic signaling pathways for plant N responses. Curr Opin Plant Biol 15:185–191
Aziz MM, Palta JA, Siddique KHM, Sadras VO (2017) Five decades of selection for yield reduced root length density and increased nitrogen uptake per unit root length in australian wheat varieties. Plant Soil 413(1–2):181–192
Beidler KV, Taylor BN, Strand AE, Cooper ER, Schönholz M, Pritchard SG (2015) Changes in root architecture under elevated concentrations of CO2 and nitrogen reflect alternate soil exploration strategies. New Phytol 205(3):1153–1163
Bohm W (1979) Methods of studying root systems. Springer, New York, pp VII–VIII
Burns I (1980) Influence of the spatial distribution of nitrate on the uptake of N by plants: a review and a model for rooting depth. J Soil Sci 31:155–173
Cahill JF, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, Clair CCS (2010) Plants integrate information about nutrients and neighbors. Science 328:1657–1657
Corre-Hellou G, Dibet A, Hauggaard-Nielsen H, Crozat Y, Gooding M, Ambus P, Dahlmann C, von Fragstein P, Pristeri A, Monti M (2011) The competitive ability of pea-barley intercrops against weeds and the interactions with crop productivity and soil N availability. Field Crops Res 122:264–272
Crawley MJ (1997) Plant ecology. Blackwell, Cambridge
Croft SA, Hodge A, Pitchford JW (2012) Optimal root proliferation strategies: the roles of nutrient heterogeneity, competition and mycorrhizal networks. Plant Soil 351:191–206
Cui M, Caldwell MM (1998) Nitrate and phosphate uptake by Agropyron desertorum and Artemisia tridentata from soil patches with balanced and unbalanced nitrate and phosphate supply. New Phytol 139:267–272
Dalal RC (1974) Effects of intercropping maize with pigeon peas on grain yield and nutrient uptake. Exp Agric 10:219–224
Desnos T (2008) Root branching responses to phosphate and nitrate. Curr Opin Plant Biol 11:82–87
Emteryd, O (1989) Chemical and physical analysis of inorganic nutrient in plant, soil, water and air. Stencil no. 10. Umea, Sweden, pp. 156–159
Gaudin A, 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
Ghosh PK (2004) Growth, yield, competition and economics of groundnut/cereal fodder intercropping systems in the semi-arid tropics of India. Field Crops Res 88:227–237
Giehl RF, Lima JE, von Wirén N (2012) Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24:33–49
Giehl RF, Gruber BD, von Wirén N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778
Gruber BD, Giehl RF, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179
Heppell J, Talboys P, Payvandi S, Zygalakis KC, Fliege J, Withers PJA, Jones DL, Roose T (2015) How changing root system architecture can help tackle a reduction in soil phosphate (P) levels for better plant P acquisition. Plant Cell Environ 38(1):118–128
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24
Hunt R (1982) Plant growth analysis. The Lavenham Press, Suffolk
Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a 14C-labeled hardwood forest. New Phytol 172:523–535
Kellermeier F, Chardon F, Amtmann A (2013) Natural variation of Arabidopsis root architecture reveals complementing adaptive strategies to potassium starvation. Plant Physiol 161:1421–1432
Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol 57(4):707–714
Li L, Sun JH, Zhang FS, Li XL, Rengel Z, Yang SC (2001a) Wheat/maize or wheat/soybean strip intercropping II. Recovery or compensation of maize and soybean after wheat harvesting. Field Crops Res 71:173–181. https://doi.org/10.1016/s0378-4290(01)00157-5
Li L, Sun JH, Zhang FS, Li XL, Yang SC, Rengel Z (2001b) Wheat/maize or wheat/soybean strip intercropping I. Yield advantage and interspecific interactions on nutrients. Field Crops Res 71:123–137. https://doi.org/10.1016/s0378-4290(01)00156-3
Li L, Sun JH, Zhang FS, Guo TW, Bao XG, Smith FA, Smith SE (2006) Root distribution and interactions between intercropped species. Oecologia 147:280–290. https://doi.org/10.1007/s00442-005-0256-4
Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci 104:11192–11196
Li L, Sun JH, Zhang FS (2011a) Intercropping with wheat leads to greater root weight density and larger below-ground space of irrigated maize at late growth stages. Soil Sci Plant Nutr 57:61–67
Li QZ, Sun JH, Wei XJ, Christie P, Zhang FS, Li L (2011b) Overyielding and interspecific interactions mediated by nitrogen fertilization in strip intercropping of maize with faba bean, wheat and barley. Plant Soil 339:147–161. https://doi.org/10.1007/s11104-010-0561-5
Liu YX, Zhang WP, Sun JH, Li XF, Peter C, Li L (2015) High morphological and physiological plasticity of wheat roots is conducive to higher competitive ability of wheat than maize in intercropping system. Plant Soil 397:387–399. https://doi.org/10.1007/s11104-015-2654-7
Madhavan M, Shanmugasundaram VS (1990) Effect of population on nutrient uptake of pigeonpea genotypes in sole and intercropped situation with sorghum CO 22. Acta Agron Hung 39:389–392
Mason SC, Leihner DE, Vorst JJ (1986) Cassava-cowpea and cassava-peanut intercropping. I. Yield and land use efficiency. Agron J 78:43–46
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo DL, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518
Mommer L, van Ruijven J, Jansen C, van de Steeg HM, de Kroon H (2012) Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory? Funct Ecol 26:66–73
Mou P, Jones RH, Tan Z, Bao Z, Chen H (2013) Morphological and physiological plasticity of plant roots when nutrients are both spatially and temporally heterogeneous. Plant Soil 364:373–384
Mu XY, Zhao YL, Liu K, Ji BY, Guo HB, Xue ZW, Li C (2016) Responses of soil properties, root growth and crop yield to tillage and crop residue management in a wheat–maize cropping system on the North China plain. Eur J Agron 78:32–43
Mucheru-Muna M, Pypers P, Mugendi D, Kung’u J, Mugwe J, Merckx R, Vanlauwe B (2010) A staggered maize–legume intercrop arrangement robustly increases crop yields and economic returns in the highlands of Central Kenya. Field Crops Res 115:132–139
Rich SM, Watt M (2013) Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. J Exp Bot 64:1193–1208
Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127:635–674
Robinson D, Linehan DJ, Gordon DC (1994) Capture of nitrate from soil by wheat in relation to root length, nitrogen inflow and availability. New Phytol 128:297–305
Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Martin-Magniette ML, Van Der Merwe MJ, Kakar K, Gouzy J, Fernie AR (2008) Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiol 146:2020–2035
SAS Institute (2011) The SAS system for windows, release 9.2. SAS Institute Inc, Cary
Van Vuuren M, Robinson D, Griffiths B (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant Soil 178:185–192
Vandermeer JH (1992) The ecology of intercropping. Cambridge University Press, New York
Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot 97:875–881
Wang YF, Qin YZ, Chai Q, Feng FX, Zhao C, Yu AZ (2018a) Interspecies interactions in relation to root distribution across the rooting profile in wheat-maize intercropping under different plant densities. Front Plant Sci 9:483. https://doi.org/10.3389/fpls.2018.00483
Wang P, Yang Y, Mou P, Zhao QZ, Li YB (2018b) Local root growth and death are mediated by contrasts in nutrient availability and root quantity between soil patches. P Roy Soc B-Biol Sci 285:20180699. https://doi.org/10.1098/rspb.2018.0699
Wiley RW (1979) Intercropping-its importance and research needs. Part1.Competition and yield advantages. Field Crops Abstr 32:1–10
Xia HY, Zhao JH, Sun JH, Bao XG, Christie P, Zhang FS, Li L (2013) Dynamics of root length and distribution and shoot biomass of maize as affected by intercropping with different companion crops and phosphorus application rates. Field Crops Res 150:52–62. https://doi.org/10.1016/j.fcr.2013.05.027
Xu BC, Li FM, Shan L (2008) Switchgrass and milkvetch intercropping under 2: 1 row-replacement in semiarid region, Northwest China: aboveground biomass and water use efficiency. Eur J Agron 28:485–492
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 FS, Li L (2003) Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant Soil 248:305–312
Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534
Zhu YY, Chen HY, Fan JH, Wang YY, Li Y, Chen JB, Fan JX, Yang SS, Hu LP, Leung H (2000) Genetic diversity and disease control in rice. Nature 406:718–722
Acknowledgements
We thank Prof. Hans Lambers for his comments and suggestions toward improving the manuscript. The research was financially supported by the National Natural Science Foundation of China (NSFC) (Project Nos. 31430014, 31270477 and 31601682) and by the National Key Research and Development Program (Project No: 2016YFD0300202).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Martin Weih.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Liu, YX., Sun, JH., Zhang, FF. et al. The plasticity of root distribution and nitrogen uptake contributes to recovery of maize growth at late growth stages in wheat/maize intercropping. Plant Soil 447, 39–53 (2020). https://doi.org/10.1007/s11104-019-04034-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-04034-9