|Local nitrogen application increases maize post-silking nitrogen uptake of responsive genotypes via enhanced deep root growth
|CHEN Zhe1, REN Wei1, YI Xia1, LI Qiang2, CAI Hong-guang3, Farhan ALI4, YUAN Li-xing1, MI Guo-hua1, PAN Qing-chun1, CHEN Fan-jun1, 2
1 College of Resources and Environmental Sciences/National Academy of Agriculture Green Development/Key Laboratory of Plant-Soil Interactions, Ministry of Education, China Agricultural University, Beijing 100193, P.R.China
2 Sanya Institute of China Agricultural University, Sanya 572025, P.R.China
3 Institute of Agricultural Resource and Environment, Jilin Academy of Agricultural Sciences, Changchun 130033, P.R.China
4 Cereal Crops Research Institute, Pirsabak Nowshera 24110, Pakistan
土壤中的氮素分布不均，在氮素富集的土壤区域内，植物根系大量的生长。然而，不同玉米基因型根系对局部施氮的响应与氮素吸收效率之间的关系尚不清楚。本研究以4个玉米品种为研究对象，探讨根系生长对局部施氮响应的基因型差异及对氮素吸收的影响。在水培采用分根培养体系局部供氮，在田间采用条施和穴施的局部施氮方法。结果表明，不同品种根系局部氮响应在水培和田间条件之间具有高度相关性（r>0.99）。在水培局部供氮条件下，强响应品种郑单958、先玉335和先锋32D22的侧根长增加了50-63%，根系生物量增加了36-53%，而弱响应品种蠡玉13的根系生长响应较小。田间条件下，3个强响应品种的根长在40-60 cm土层显著增加66-75%，而蠡玉13的根长变化幅度显著较低。此外，局部施氮肥促进强响应品种的花后氮吸收，增幅达16-88%，并且促进了郑单958的籽粒产量显著增加10-12%。相关分析发现，产量与40-60 cm土层根长呈显著正相关（r=0.39）。综上所述，可在苗期鉴定玉米品种对局部施氮的响应类型，生产中强响应型玉米品种与局部施用氮肥配套应用；同时可将“根系局部施氮响应能力”作为玉米氮高效遗传改良的目标性状。
Nitrogen (N) is unevenly distributed throughout the soil and plant roots proliferate in N-rich soil patches. However, the relationship between the root response to localized N supply and maize N uptake efficiency among different genotypes is unclear. In this study, four maize varieties were evaluated to explore genotypic differences in the root response to local N application in relation to N uptake. A split-root system was established for hydroponically-grown plants and two methods of local N application (local banding and local dotting) were examined in the field. Genotypic differences in the root length response to N were highly correlated between the hydroponic and field conditions (r>0.99). Genotypes showing high response to N, ZD958, XY335 and XF32D22, showed 50‒63% longer lateral root length and 36‒53% greater root biomass in N-rich regions under hydroponic conditions, while the LY13 genotype did not respond to N. Under field conditions, the root length of the high-response genotypes was found to increase by 66‒75% at 40‒60 cm soil depth, while LY13 showed smaller changes in root length. In addition, local N application increased N uptake at the post-silking stage by 16‒88% in the high-response genotypes and increased the grain yield of ZD958 by 10‒12%. Moreover, yield was positively correlated with root length at 40‒60 cm soil depth (r=0.39). We conclude that local fertilization should be used for high-response genotypes, which can be rapidly identified at the seedling stage, and selection for “local-N responsive roots” can be a promising trait in maize breeding for high nitrogen uptake efficiency.
Received: 29 January 2022
Accepted: 31 March 2022
This work was financially supported by the Hainan Provincial Natural Science Foundation of China (321CXTD443) and the National Natural Science Foundation of China (31972485 and 31971948).
|About author: Received 29 January, 2022 Accepted 31 March, 2022
CHEN Zhe, E-mail: email@example.com; Correspondence CHEN Fan-jun, Tel: +86-10-62734454, E-mail: firstname.lastname@example.org
Cite this article:
CHEN Zhe, REN Wei, YI Xia, LI Qiang, CAI Hong-guang, Farhan ALI, YUAN Li-xing, MI Guo-hua, PAN Qing-chun, CHEN Fan-jun.
Local nitrogen application increases maize post-silking nitrogen uptake of responsive genotypes via enhanced deep root growth. Journal of Integrative Agriculture, 22(1): 235-250.
| Arai-Sanoh Y, Takai T, Yoshinaga S, Nakano H, Kojima M, Sakakibara H, Kondo M, Uga Y. 2014. Deep rooting conferred by DEEPER ROOTING 1 enhances rice yield in paddy fields. Scientific Reports, 4, 5563.
Bloom A J. 1997. Nitrogen as a limiting factor: crop acquisition of ammonium and nitrate. In: Jackson L E, ed., Ecology in Agriculture. Academic Press, San Diego, US. pp. 145–172.
Bouguyon E, Brun F, Meynard D, Kubes M, Pervent M, Leran S, Lacombe B, Krouk G, Guiderdoni E, Zazimalova E, Hoyerova K, Nacry P, Gojon A. 2015. Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nature Plants, 1, 15015.
Bouguyon E, Perrine-Walker F, Pervent M, Rochette J, Cuesta C, Benkova E, Martinière A, Bach L, Krouk G, Gojon A. 2016. Nitrate controls root development through posttranscriptional regulation of the NRT1.1/NPF6.3 transporter/sensor. Plant Physiology, 172, 1237–1248.
Chapman N, Miller A J, Lindsey K, Whalley W R. 2012. Roots, water, and nutrient acquisition: let’s get physical. Trends in Plant Science, 17, 701–710.
Chen X P, Cui Z L, Fan M S, Vitousek P, Zhao M, Ma W Q, Wang Z L, Zhang W J, Yan X Y, Yang J X, Deng X P, Gao Q, Zhang Q, Guo S W, Ren J, Li S Q, Ye Y L, Wang Z H, Huang J L, Tang Q Y, et al. 2014. Producing more grain with lower environmental costs. Nature, 514, 486–489.
Chen Z, Sun J L, Li D D, Li P C, He K H, Ali F, Mi G H, Chen F J, Yuan L X, Pan Q C. 2022. Plasticity of root anatomy during domestication of a maize-teosinte derived population. Journal of Experimental Botany, 72, 139–153.
Chen Z, Yi X, Chen F J, Mi G H, Tian P, Qi H. 2017. Differential response of maize roots to heterogeneous local nitrogen and phosphorus supply and genotypic differences. Journal of Plant Nutrition and Fertilizer, 23, 83–90. (in Chinese)
Cheng Y, Wang H Q, Liu P, Dong S T, Zhang J W, Zhao B, Ren B Z. 2020. Nitrogen placement at sowing affects root growth, grain yield formation, N use efficiency in maize. Plant and Soil, 457, 355–373.
Drew M. 1975. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist, 75, 479–490.
Drew M C, Saker L R. 1975. Nutrient supply and the growth of the seminal root system in barley. 2. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. Journal of Experimental Botany, 26, 79–90.
Erisman J W, Sutton M A, Galloway J, Klimont Z, Winiwarter W. 2008. How a century of ammonia synthesis changed the world. Nature Geoscience, 1, 636–639.
Feng G Z, Yan L, Wang Y, Wang S J, Li J H, Chen X P, Cui Z L, Fan X L, Gao Q. 2017. Establishment of index system of fertilizer recommendation for spring maize in Jilin. Journal of Maize Sciences, 25, 142–147. (in Chinese)
Fransen B. 1999. Root Foraging: The Consequences for Nutrient Acquisition and Competition in Heterogeneous Environments. Wageningen University, Wageningen.
Fransen B, de Kroon H, Berendse F. 1998. Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia, 115, 351–358.
Garnett T, Plett D, Conn V, Conn S, Rabie H, Rafalski J A, Dhugga K, Tester M A, Kaiser B N. 2015. Variation for N uptake system in maize: Genotypic response to N supply. Frontiers in Plant Science, 6, 936.
Giehl R F, von-Wiren N. 2014. Root nutrient foraging. Plant Physiology, 166, 509–517.
Guan P, Wang R, Nacry P, Breton G, Kay S A, Pruneda-Paz J L, Davani A, Crawford N M. 2014. Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 111, 15267–15272.
Guo Y F, Chen F J, Zhang F S, Mi G H. 2005b. Auxin transport from shoot to root is involved in the response of lateral root growth to localized supply of nitrate in maize. Plant Science, 169, 894–900.
Guo Y F, Mi G H, Chen F J, Zhang F S. 2005a. Genotype difference of maize lateral roots in response to local nitrate supply. Plant Nutrition and Fertilizer Science, 11, 155–159. (in Chinese)
Ham B K, Chen J, Yan Y, Lucas W J. 2018. Insights into plant phosphate sensing and signaling. Current Opinion in Biotechnology, 49, 1–9.
Hammer G L, Dong Z S, McLean G, Doherty A, Messina C, Schussler J, Zinselmeier C, Paszkiewicz S, Cooper M. 2009. Can changes in canopy and/or root system architecture explain historical maize yield trends in the U.S. corn belt? Crop Science, 49, 299–312.
Hirel B. 2001. Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiology, 125, 1258–1270.
Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist, 162, 9–24.
Huang G, Yi K K, Wu Y R, Zhu L, Mao C Z, Wu P. 2004. QTLs for nitrate induced elongation and initiation of lateral roots in rice (Oryza sativa L.). Plant and Soil, 263, 229–237.
Jia Z T, Giehl R F H, von Wirén N. 2021. Nutrient-hormone relations: Driving root plasticity in plants. Molecular Plants, 15, 86–103.
Jia Z T, von Wirén N. 2020. Signaling pathways underlying nitrogen-dependent changes in root system architecture: From model to crop species. Journal of Experimental Botany, 71, 4393–4403.
Jin K M, Shen J B, Ashton R W, White R P, Dodd I C, Parry M A J, Whalley W R. 2015. Wheat root growth responses to horizontal stratification of fertilizer in a water-limited environment. Plant and Soil, 386, 77–88.
Jing J Y, Gao W, Cheng L Y, Wang X, Duan F Y, Yuan L X, Rengel Z, Zhang F S, Li H G, Cahill Jr J F, Shen J B. 2022. Harnessing root-foraging capacity to improve nutrient-use efficiency for sustainable maize production. Field Crops Research, 279, 108462.
Jing J Y, Rui Y, Zhang F S, Rengel Z, Shen J B. 2010. Localized application of phosphorus and ammonium improves growth of maize seedlings by stimulating root proliferation and rhizosphere acidification. Field Crops Research, 119, 355–364.
Ju X T, Xing G, Chen X P, Zhang S, Zhang L, Liu X, Cui Z L, Yin B, Christie P, Zhu Z, Zhang F S. 2009. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proceedings of the National Academy of Sciences of the United States of America, 106, 3041–3046.
Ju X T, Zhang C. 2017. Nitrogen cycling and environmental impacts in upland agricultural soils in North China: A review. Journal of Integrative Agriculture, 16, 2848–2862.
Kembel S W, De Kroon H, James F, Cahill J, Mommer L. 2008. Improving the scale and precision of hypotheses to explain root foraging ability. Annals of Botany, 101, 1295–1301.
Kiba T, Kudo T, Kojima M, Sakakibara H. 2011. Hormonal control of nitrogen acquisition: Roles of auxin, abscisic acid, and cytokinin. Journal of Experimental Botany, 62, 1399–1409.
Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim K Y, Kwon M, Endler A, Song W . 2014. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proceedings of the National Academy of Sciences of the United States of America, 111, 7150–7155.
Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell, 18, 927–937.
Li H B, Wang X, Rengel Z, Ma Q H, Zhang F S, Shen J B. 2016. Root over-production in heterogeneous nutrient environment has no negative effects on Zea mays shoot growth in the field. Plant and Soil, 409, 1–13.
Li P C, Yang X Y, Wang H M, Pan T, Wang Y Y, Xu Y, Xu C W, Yang Z F. 2021. Genetic control of root plasticity in response to salt stress in maize. Theoretical and Applied Genetics, 134, 1–18.
Linkohr B I, Williamson L C, Fitter A H, Leyser H M. 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant Journal, 29, 751–760.
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. Annals of Botany, 106, 1019–1026.
Liu J, Fernie A R, Yan J B. 2020. The past, present, and future of maize improvement: Domestication, genomics, and functional genomic routes toward crop enhancement. Plant Communications, 1, 1–19.
Liu J X, Han L L, Chen F J, Bao J, Zhang F S, Mi G H. 2008. Microarray analysis reveals early responsive genes possibly involved in localized nitrate stimulation of lateral root development in maize (Zea mays L.). Plant Science, 175, 272–282.
Liu X J, Vitousek P, Chang Y H, Zhang W F, Matson P, Zhang F S. 2016. Evidence for a historic change occurring in China. Environmental Science & Technology, 50, 505–506.
Liu Y, Jia Z T, Li X L, Wang Z K, Chen F J, Mi G H, Forde B G, Takahashi H, Yuan L X. 2020. Involvement of a truncated MADS-box transcription factor ZmTMM1 in root nitrate foraging. Journal of Experimental Botany, 71, 4547–4561.
Liu Y, von-Wirén N. 2022. Integration of nutrient and water availabilities via auxin into the root developmental program. Current Opinion of Plant Biology, 65, 102117.
Lynch J P. 2013. Steep, cheap and deep: An ideotype to optimize water and N acquisition by maize root systems. Annals of Botany, 112, 347–357.
Lynch J P. 2019. Root phenotypes for improved nutrient capture: An underexploited opportunity for global agriculture. New Phytologist, 223, 548–564.
Lynch J P, Tobias W. 2015. Opportunities and challenges in the subsoil: pathways to deeper rooted crops. Journal of Experimental Botany, 66, 2199–2210.
Ma Q H, Wang X, Li H B, Li H G, Zhang F S, Rengel Z, Shen J B. 2015. Comparing localized application of different N fertilizer species on maize grain yield and agronomic N-use efficiency on a calcareous soil. Field Crops Research, 180, 72–79.
Maghiaoui A, Bouguyon E C, Cuesta F P W, Section C, Alcon G, Krouk E, Benkova P, Nacry A, Gojon, Bach L. 2020. The Arabidopsis NRT1.1 transceptor coordinately controls auxin biosynthesis and transport to regulate root branching in response to nitrate. Journal of Experimental Botany, 71, 4480–4494.
Mc-Cleery W T, Mohd-Radzman N A, Grieneisen V A. 2017. Root branching plasticity: Collective decision-making results from local and global signaling. Current Opinion in Cell Biology, 44, 51–58.
Mi G H, Chen F J, Wu Q P, Lai N W, Yuan L X, Zhang F S. 2010. Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Science China Life Sciences, 53, 1369–1373.
Mi G H, Chen F J, Yuan L X, Zhang F S. 2016. Ideotype root system architecture for maize to achieve high yield and resource use efficiency in intensive cropping systems. Advances in Agronomy, 139, 73–97.
Mu X H, Chen F J, Wu Q P, Chen Q W, Wang J F, Yuan L X, Mi G H. 2015. Genetic improvement of root growth increases maize yield via enhanced post-silking nitrogen uptake. European Journal of Agronomy, 63, 55–61.
Nelson D W, Sommers L E. 1973. Determination of total nitrogen in plant material. Agronomy Journal, 65, 109–112.
Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y. 2017. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nature Plants, 3, 17029.
Poitout A, Crabos A, Petřík I, Novák O, Krouk G, Lacombe B, Ruffel S. 2018. Responses to systemic nitrogen signaling in Arabidopsis roots involve trans-zeatin in shoots. The Plant Cell, 30, 1243–1257.
Robinson D. 1996. Resource capture by localized root proliferation: Why do plants bother? Annals of Botany, 77, 179–185.
Ruffel S. 2018. Nutrient-related long-distance signals: Common players and possible cross-talk. Plant and Cell Physiology, 59, 1723–1732.
Ruidisch M, Bartsch S, Kettering J, Huwe B, Frei S. 2013. The effect of fertilizer best management practices on nitrate leaching in a plastic mulched ridge cultivation system. Agriculture, Ecosystems and Environment, 169, 21–32.
Sattelmacher B, Thomas K. 2010. Morphology and physiology of the seminal root system of young maize (Zea mays L.) plants as influenced by a locally restricted nitrate supply. Journal of Soil Science and Plant Nutrition, 158, 493–497.
Schneider H M, Lor V S N, Hanlon M T, Perkins A, Kaeppler S M, Bhosale R, Borkar A N, Zhang X, Riodriguez J, Bucksch A, Bennett M J, Brown K M, Lynch J P. 2022. Root angle in maize influences nitrogen capture and is regulated by calcineurin B-like protein (CBL)-interacting serine/threonine-protein kinase 15 (ZmCIPK15). Plant Cell and Environment, 45, 837–853.
Schneider N, Klein S, Hanlon M T, Nord E A, Kaeppler S M, Brown K M, Warry A, Bhosale R A, Lynch J P. 2020. Genetic control of root architectural plasticity in maize. Journal of Experimental Botany, 71, 3185–3197.
Shao H, Shi D F, Shi W J, Ban X B, Chen Y C, Ren W, Chen F J, Mi G H. 2019. Genotypic difference in the plasticity of root system architecture of field-grown maize in response to plant density. Plant and Soil, 439, 201–217.
Soil Survey Staff. 1998. Keys to Soil Taxonomy. United States Department of Agriculture, Natural Resources Conservation Service, Washington D.C. pp. 326.
Sun X C, Ren W, Wang P, Chen F J, Yuan L J, Pan Q C, Mi G H. 2021. Evaluation of maize root growth and genome-wide association studies of root traits in response to low nitrogen supply at seedling emergence. The Crop Journal, 9, 794–804.
Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science, 346, 343–346.
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J Z, Matsumoto T, Takai T, Okuno K, Yano M. 2013. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics, 45, 1097–1102.
Wang P, Wang Z K, Pan Q C, Sun X C, Mi G H. 2019. Increased biomass accumulation in maize grown in mixed nitrogen supply is mediated by auxin synthesis. Journal of Experimental Botany, 70, 1859–1873.
Wang X, Feng J, White P J, Shen J, Chen L. 2020a. Heterogeneous phosphate supply influences maize lateral root proliferation by regulating auxin redistribution. Annals of Botany, 125, 119–130.
Wang X, Whalley W R, Miller A J, White P J, Zhang F S, Shen J B. 2020b. Sustainable cropping requires adaptation to a heterogeneous rhizosphere. Trends in Plant Science, 25, 1194–1202.
Xu G H, Fan X R, Miller A J. 2012. Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology, 63, 153–182.
Yu P, Li X X, White P J, Li C J. 2015. A large and deep root system underlies high nitrogen-use efficiency in maize production. PLoS ONE, 10, e0126293.
Yu P, Li X X, Yuan L X, Li C J. 2014b. A novel morphological response of maize (Zea mays) adult roots to heterogeneous nitrate supply revealed by a split-root experiment. Physiologia Plantarum, 150, 133–144.
Yu P, White P J, Hochholdinger F, Li C J. 2014a. Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta, 240, 667–678.
Zhai X F, Zhou J X, Sun H R, Tang L, Shen Y F. 2019. Effects of localized high nitrate supply on maize roots morphology and N accumulation. Agricultural Research in the Arid Areas, 4, 91–99. (in Chinese)
Zhang H, Jennings A, Barlow P W, Forde B G. 1999. Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America, 96, 6529–6534.
Zhang X, Davidson E A, Mauzerall D L, Searchinger T D, Dumas P, Shen Y. 2015. Managing nitrogen for sustainable development. Nature, 528, 51–59.
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