Please wait a minute...
Journal of Integrative Agriculture  2014, Vol. 13 Issue (11): 2508-2517    DOI: 10.1016/S2095-3119(13)60523-7
Soil & Fertilization · Irrigation · Agro-Ecology & Environment Advanced Online Publication | Current Issue | Archive | Adv Search |
Cell Production and Expansion in the Primary Root of Maize in Response to Low-Nitrogen Stress
 GAO Kun, CHEN Fan-jun, YUAN Li-xing , MI Guo-hua
Key Laboratory of Plant-Soil Interaction, Ministry of Agriculture/Center for Resources, Environment and Food Security, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  Maize plants respond to low-nitrogen stress by enhancing root elongation. The underlying physiological mechanism remains unknown. Seedlings of maize (Zea mays L., cv. Zhengdan 958) were grown in hydroponics with the control (4 mmol L-1) or low-nitrogen (40 μmol L-1) for 12 d, supplied as nitrate. Low nitrogen enhanced root elongation rate by 4.1-fold, accompanied by increases in cell production rate by 2.2-fold, maximal elemental elongation rate (by 2.5-fold), the length of elongation zone (by 1.5-fold), and final cell length by 1.8-fold. On low nitrogen, the higher cell production rate resulted from a higher cell division rate and in fact the number of dividing cells was reduced. Consequently, the residence time of a cell in the division zone tended to be shorter under low nitrogen. In addition, low nitrogen increased root diameter, an increase that occurred specifically in the cortex and was accompanied by an increase in cell number. It is concluded that roots elongates in response to low-nitrogen stress by accelerating cell production and expansion.

Abstract  Maize plants respond to low-nitrogen stress by enhancing root elongation. The underlying physiological mechanism remains unknown. Seedlings of maize (Zea mays L., cv. Zhengdan 958) were grown in hydroponics with the control (4 mmol L-1) or low-nitrogen (40 μmol L-1) for 12 d, supplied as nitrate. Low nitrogen enhanced root elongation rate by 4.1-fold, accompanied by increases in cell production rate by 2.2-fold, maximal elemental elongation rate (by 2.5-fold), the length of elongation zone (by 1.5-fold), and final cell length by 1.8-fold. On low nitrogen, the higher cell production rate resulted from a higher cell division rate and in fact the number of dividing cells was reduced. Consequently, the residence time of a cell in the division zone tended to be shorter under low nitrogen. In addition, low nitrogen increased root diameter, an increase that occurred specifically in the cortex and was accompanied by an increase in cell number. It is concluded that roots elongates in response to low-nitrogen stress by accelerating cell production and expansion.
Keywords:  cell length       elemental expansion       kinematic analysis       root diameter       root elongation       Zea mays L.  
Received: 08 April 2013   Accepted: 14 November 2014
Fund: 

This work was financially supported by the National Natural Science Foundation of China (31071852 and 31121062). We thank Professor Tobias I Baskin (University of Massachusetts Amherst, USA) for the critical comments on the kinematic analysis and great assistance in manuscript preparation.

Corresponding Authors:  MI Guo-hua, E-mail: miguohua@cau.edu.cn     E-mail:  miguohua@cau.edu.cn
About author:  GAO Kun, Mobile: 15810536392, E-mail: happycreek@126.com

Cite this article: 

GAO Kun, CHEN Fan-jun, YUAN Li-xing , MI Guo-hua. 2014. Cell Production and Expansion in the Primary Root of Maize in Response to Low-Nitrogen Stress. Journal of Integrative Agriculture, 13(11): 2508-2517.

Baskin T I, Cork A, Williamson R E, Gorst J R. 1995.STUNTED PLANT 1, a gene required for expansion inrapidly elongating but not in dividing cells and mediatingroot growth responses to applied cytokinin. PlantPhysiology, 107, 233-243

Baskin T I, Remillong E L, Wilson J E. 2001. The impactof mannose and other carbon sources on the elongationand diameter of the primary root of Arabidopsis thaliana.Australian Journal of Plant Physiology, 8, 481-488

Baskin T I. 2013. Patterns of root growth acclimation: Constantprocesses, changing boundaries. WIREs DevelopmentalBiology, 2, 65-73

Beemster G T S, Baskin T I. 1998. Analysis of cell divisionand elongation underlying the developmental accelerationof root growth in Arabidopsis thaliana. Plant Physiology,116, 1515-1526

Beemster G T S, Baskin T I. 2000. STUNTED PLANT 1mediates effects of cytokinin, but not of auxin, on celldivision and expansion in the root of Arabidopsis. PlantPhysiology, 124, 1718-1727

Beman J M, Arrigo K R, Matson P A. 2005. Agricultural runofffuels large phytoplankton blooms in vulnerable areas ofthe ocean. Nature, 434, 211-214

Bengough A G, McKenzie B, Hallett P, Valentine T. 2011.Root elongation, water stress, and mechanical impedance:A review of limiting stresses and beneficial root tip traits.Journal of Experimental Botany, 62, 59-68

Bosemark N O. 1954. The influence of nitrogen on rootdevelopment. Physiologia Plantarum, 7, 497-502

Clark L J, Price A H, Steele K A, Whalley W R. 2008. Evidencefrom near-isogenic lines that root penetration increaseswith root diameter and bending stiffness in rice. FunctionalPlant Biology, 35, 1163-1171

De Cnodder T, Verbelen J P, Vissenberg K. 2007. The controlof cell size and rate of elongation in the Arabidopsisroot. In: Plant Cell Monographs. 5th ed. Springer, BerlinHerdelberg. pp. 249-269

Darzynkiewicz Z, Andreef M, Tranganos F, Sharpless T,Melamed M R. 1978. Discrimination of cycling and noncyclinglymphocytes by BUdR-suppressed acridine orangefluorescence in a flow cytometric system. ExperimentalCell Research, 115, 31-35

Dewitte W, Riou-Khamlichi C, Scofield S, Healy J M S,Jacqmard A, Kilby N J, Murray J A H. 2003. Altered cellcycle distribution, hyperplasia, and inhibited differentiationin Arabidopsis caused by the D-type cyclin CYCD3. ThePlant Cell Online, 15, 79-92

Downes B P, Steinbaker C R, Crowell D N. 2001. Expressionand processing of a hormonally regulated β-expansin fromsoybean. Plant Physiology, 126, 244-252

Flynn K, Davidson K, Leftley J. 1994. Carbon-nitrogenat whole-cell and free-amino-acid levels during batchgrowth of Isochrysis galbana (Prymnesiophyceae) underconditions of alternating light and dark. Marine Biology,118, 229-237

Gastal F, Nelson C J. 1994. Nitrogen use within the growingleaf blade of tall fescue. Plant Physiology, 105, 191-197

Gaudin A C M, McClymont S A, Holmes B M, Lyons E,Raizada M N. 2011. Novel temporal, fine-scale and growthvariation phenotypes in roots of adult-stage maize (Zeamays L.) in response to low nitrogen stress. Plant, Celland Environment, 34, 2122-2137

Greef J M, Geisler G. 1988. Growth of isolated maize root tipsat various levels of N supply. Mitteilungen der Gesellschaftfur Pflanzenbauwissenschaften, 1, 63-65

Hirel B, Le Gouis J, Ney B, Gallais A. 2007. The challengeof improving nitrogen use efficiency in crop plants:Towards a more central role for genetic variability andquantitative genetics within integrated approaches. Journalof Experimental Botany, 58, 2369-2387

Itoh S, Barber S A. 1983. Phosphorus uptake by six plantspecies as related to root hairs. Agronomy Journal, 75,457-461

Ivanov V B, Dubrovsky J G. 1997. Estimation of the cellcycleduration in the root apical meristem: A model oflinkage between cell-cycle duration, rate of cell production,and rate of root growth. International Journal of PlantSciences, 158, 757-763

Kavanová M, Lattanzi F A, Grimoldi A A, Schnyder H.2006. Phosphorus deficiency decreases cell division andelongation in grass leaves. Plant Physiology, 141, 766-775

Kavanová M, Lattanzi F A, Schnyder H. 2008. Nitrogendeficiency inhibits leaf blade growth in Lolium perenne byincreasing cell cycle duration and decreasing mitotic andpost-mitotic growth rates. Plant, Cell and Environment,31, 727-737

Kiba T, Kudo T, Kojima M, Sakakibara H. 2011. Hormonalcontrol of nitrogen acquisition: roles of auxin, abscisicacid, and cytokinin. Journal of Experimental Botany, 62,1399-1409

Kubica Š, Baluška F. 1988. Maize primary root growth anddifferentiation under conditions of nitrate over-supply.Biológia (Bratislava), 44, 407-414

Li Q, Li B H, Kronzucker H J, Shi W M. 2010. Root growthinhibition by NH4+ in Arabidopsis is mediated by the roottip and is linked to NH4+ efflux and GMPase activity. Plant, Cell and Environment, 33, 1529-1542

London J G. 2005. Nitrogen study fertilizes fears of pollution.Nature, 433, 791-791

Lynch J P. 2007. Roots of the second green revolution.Australian Journal of Botany, 55, 493-512

Lynch J. 1995. Root architecture and plant productivity. PlantPhysiology, 109, 7-13

Morris A K, Silk W K. 1992. Use of a flexible logistic functionto describe axial growth of plants. Bulletin of MathematicalBiology, 54, 1069-1081

Del Pozo J C, Lopez-Matas M, Ramirez-Parra E, Gutierrez C.2004. Hormonal control of the plant cell cycle. PhysiologiaPlantarum, 123, 173-183

Rahayu Y S, Walch-Liu P, Neumann G, Römheld V, VonWirén N, Bangerth F. 2005. Root-derived cytokinins aslong-distance signals for NO3--induced stimulation of leafgrowth. Journal of Experimental Botany, 56, 1143-1152

Roggatz U, McDonald A, Stadenberg I, Schurr U. 1999.Effects of nitrogen deprivation on cell division andexpansion in leaves of Ricinus communis L. Plant, Celland Environment, 22, 81-89

Rounds C M, Lubeck E, Hepler P K, Winship L J. 2011.Propidium Iodide competes with Ca2+ to label pectin inpollen tubes and Arabidopsis root hairs. Plant Physiology,157, 175-187

Sharp R E, Silk W K, Hsiao T C. 1988. Growth of the maizeprimary root at low water potentials. 1. Spatial distributionof expansive growth. Plant Physiology, 87, 50-57

Silk W K, Lord E M, Eckard K J. 1989. Growth patternsinferred from anatomical records empirical tests usinglongisections of roots of Zea mays L. Plant Physiology,90, 708-713

Silk W K. 1992. Steady form from changing cells. InternationalJournal of Plant Sciences, 153, 49-58

Thaler P, Pages L. 1996. Root apical diameter and rootelongation rate of rubber seedlings (Hevea brasiliensis)show parallel responses to photoassimilate availability.Physiologia Plantarum, 97, 365-371

Tian Q Y, Chen F J, Liu J X, Zhang F S, Mi G H. 2008.Inhibition of maize root growth by high nitrate supply iscorrelated with reduced IAA levels in roots. Journal ofPlant Physiology, 165, 942-951

Tian Q Y, Chen F J, Zhang F S, Mi G H. 2005. Possibleinvolvement of cytokinin in nitrate-mediated root growthin maize. Plant and Soil, 277, 185-196

De Veylder L, Beeckman T, Beemster G T S, Krols L, TerrasF, Landrieu I, Van Der Schueren E, Maes S, Naudts M,Inzé D. 2001. Functional analysis of cyclin-dependentkinase inhibitors of Arabidopsis. The Plant Cell Online,13, 1653-1668

Wang Y, Mi G H, Chen F J, Zhang J H, Zhang F S. 2004.Response of root morphology to nitrate supply and itscontribution to nitrogen accumulation in maize. Journalof Plant Nutrition, 27, 2189-2202

Yamaguchi M, Valliyodan B, Zhang J, Lenobie M E, Yu O,Rogers E E, Nguyen H T, Sharp R E. 2010. Regulation ofgrowth response to water stress in the soybean primary root.I. Proteomic analysis reveals region-specific regulation ofphenylpropanoid metabolism and control of free iron in theelongation zone. Plant, Cell and Environment, 33, 223-243
[1] DU Kang, ZHAO Wen-qing, ZHOU Zhi-guo, SHAO Jing-jing, HU Wei, KONG Ling-jie, WANG You-hua. Hormonal changes play important roles in the key period of superior and inferior earshoot differentiation in maize[J]. >Journal of Integrative Agriculture, 2021, 20(12): 3143-3155.
[2] XIN Yuan-yuan, Anisur RAHMAN, LI Hui-xiu, XU Ting, DING Guo-chun, LI Ji. Modification of total and phosphorus mineralizing bacterial communities associated with Zea mays L. through plant development and fertilization regimes[J]. >Journal of Integrative Agriculture, 2021, 20(11): 3026-3038.
[3] HAO Lu-yang, LIU Xu-yang, ZHANG Xiao-jing, SUN Bao-cheng, LIU Cheng, ZHANG Deng-feng, TANG Huai-jun, LI Chun-hui, LI Yong-xiang, SHI Yun-su, XIE Xiao-qing, SONG Yan-chun, WANG Tian-yu, LI Yu .
Genome-wide identification and comparative analysis of drought related genes in roots of two maize inbred lines with contrasting drought tolerance by RNA sequencing
[J]. >Journal of Integrative Agriculture, 2020, 19(2): 449-464.
[4] Jan Bocianowski, Piotr Szulc, Kamila Nowosad. Soil tillage methods by years interaction for dry matter of plant yield of maize (Zea mays L.) using additive main effects and multiplicative interaction model[J]. >Journal of Integrative Agriculture, 2018, 17(12): 2836-2839.
[5] LIU Xiao-min, XU Xian, LI Bing-hua, YAO Xiao-xia, ZHANG Huan-huan, WANG Gui-qi, HAN Yu-jun. Genomic and transcriptomic insights into cytochrome P450 monooxygenase genes involved in nicosulfuron tolerance in maize (Zea mays L.)[J]. >Journal of Integrative Agriculture, 2018, 17(08): 1790-1799.
[6] ZHOU Yu-qian, WANG Qin-yang, ZHAO Hai-liang, GONG Dian-ming, SUN Chuan-long, REN Xue-mei, LIU Zhong-xiang, HE Hai-jun, QIU Fa-zhan. Unravelling transcriptome changes between two distinct maize inbred lines using RNA-seq[J]. >Journal of Integrative Agriculture, 2018, 17(07): 1574-1584.
[7] WANG Nan, LI Liang, GAO Wen-wei, WU Yong-bo, YONG Hong-jun, WENG Jian-feng, LI Ming-shun, ZHANG De-gui, HAO Zhuan-fang, LI Xin-hai. Transcriptomes of early developing tassels under drought stress reveal differential expression of genes related to drought tolerance in maize[J]. >Journal of Integrative Agriculture, 2018, 17(06): 1276-1288.
[8] SHEN Li-xia, HUANG Yan-kai, LI Ting. Top-grain filling characteristics at an early stage of maize (Zea mays L.) with different nitrogen use efficiencies[J]. >Journal of Integrative Agriculture, 2017, 16(03): 626-639.
[9] ZHANG Dong-feng, ZHANG Nan, ZHONG Tao, WANG Chao, XU Ming-liang, YE Jian-rong. Identification and characterization of the GH3 gene family in maize[J]. >Journal of Integrative Agriculture, 2016, 15(2): 249-261.
[10] WEI Shan-shan, WANG Xiang-yu, LIU Peng, ZHANG Ji-wang, ZHAO Bin, DONG Shu-ting. Comparative proteomic analysis provides new insights into ear leaf senescence of summer maize (Zea mays L.) under fild condition[J]. >Journal of Integrative Agriculture, 2016, 15(05): 1005-1016.
[11] LIN Li-rong, HE Yang-bo, CHEN Jia-zhou. The inflence of soil drying- and tillage-induced penetration resistance on maize root growth in a clayey soil[J]. >Journal of Integrative Agriculture, 2016, 15(05): 1112-1120.
[12] WU Xiao-jun, Xu Li, ZHAO Pan-feng, LI Na, WU Lei, HE Yan, WANG Shou-cai. Comparative transcriptome profiling of two maize near-isogenic lines differing in the allelic state for bacterial brown spot disease resistance[J]. >Journal of Integrative Agriculture, 2015, 14(4): 610-621.
[13] MING Bo, GUO Yin-qiao, TAO Hong-bin, LIU Guang-zhou, LI Shao-kun, WANG Pu. SPEIPM-based research on drought impact on maize yield in North China Plain[J]. >Journal of Integrative Agriculture, 2015, 14(4): 660-669.
[14] ZHONG Wen-juan, ZHANG Mei-dong, YANG Liu-qi, WANG Ming-chun, ZHENG Yong-lian, YANG Wenpeng GAO You-jun. Isolating the Mutator Transposable Element Insertional Mutant Gene mio16 ofMaize UsingDoubleSelectedAmplification of Insertion Flanking Fragments (DSAIFF)[J]. >Journal of Integrative Agriculture, 2012, 12(10): 1592-1600.
[15] LV Ai-zhi, ZHANG Hao, ZHANG Zu-xin, TAO Yong-sheng, YUE Bing , ZHENG Yong-lian. Conversion of the Statistical Combining Ability into a Genetic Concept[J]. >Journal of Integrative Agriculture, 2012, 12(1): 43-52.
No Suggested Reading articles found!