Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (12): 2703-2715    DOI: 10.1016/S2095-3119(19)62595-5
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Differential responses of root growth to nutrition with different ammonium/nitrate ratios involve auxin distribution in two tobacco cultivars
MENG Lin1*, DONG Jian-xin1*, WANG Shu-sheng1, SONG Ke1, LING Ai-fen2, YANG Jin-guang1, XIAO Zhi-xin3, LI Wei4, SONG Wen-jing1, LIANG Hong-bo1
1 Key Laboratory of Tobacco Biology and Processing, Ministry of Agriculture and Rural Affairs/Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, P.R.China
2 Liangshan Branch of Sichuan Tobacco Corporation, Xichang 615000, P.R.China
3 Baoshan Branch, Yunnan Tobacco Company, Baoshan 678000, P.R.China
4 Hongyunhonghe Tobacco (Group) Co., Ltd., Kunming 650231, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  Nitrogen (N), the major forms of which are nitrate (NO3) and ammonium (NH4+), plays an important role in plant growth and mediation of root development.  However, the role of auxin in root growth in response to different NH4+/NO3 ratios remains unclear.  Two tobacco cultivars (Nicotiana tabacum L.) were adopted in this study, which displayed variant growth features under the situations with sole NO3 nutrition ratio (NH4+/NO3 ratio: 0/100), low NO3 nutrition ratio (NH4+/NO3ratio: 97/3), and optimal NH4+/NO3 ratio (50/50).  We investigated the effects of the different NH4+/NO3ratios on the formation and elongation of lateral roots (LRs), auxin concentration, DR5::GUS expression, 3H-labeled indole acetic acid ([3H]IAA) transport, and the expression of six PIN genes in tobacco roots.  We also examined the effects of exogenous auxin and a transport inhibitor on LRs growth.  The results are shown as follows, compared to optimal N nutrition conditions, the biomass and nitrogen (N) accumulation were largely reduced by sole and low NO3 nutrition treatment in NC89, but no difference was observed in Zhongyan 100.  In most cases, sole and low NO3 nutrition impaired the elongation and formation of first-order lateral roots (1° LRs), only in NC89, thus reducing the root growth.  IAA concentration and DR5::GUS expression levels decreased in roots when NC89 was subjected to sole and low NO3 nutrition media, suggesting that different NH4+/NO3 ratios affect the transport of auxin from leaves to roots.  Results were similar following exogenous NAA application to low NO3 nutrition treated seedlings.  Based on direct [3H]IAA transport measurement, the transport of polar auxin from shoots to roots decreased due to low NO3nutrition.  PIN4 expression levels were markedly decreased in roots of NC89 by sole and low NO3 nutrition, while they were unaffected in Zhongyan 100 roots.  Overall, our findings suggest that LRs formation in tobacco seedlings is regulated by NH4+/NO3 ratios via modifying polar transport of auxin.
 
Keywords:  auxin        lateral root        formation and elongation        tobacco        NH4+/NO3 ratio  
Received: 23 July 2018   Accepted:
Fund: This work was funded by the Agricultural Science and Technology Innovation Program, Chinese Academy of Agricultural Sciences (ASTIP-TRIC03), the Science Foundation for Young Scholars of Tobacco Research Institute of Chinese Academy of Agricultural Sciences (2018B01), the National Nature Science Foundation of China (3601818), the Liangshan Branch of Sichuan Tobacco Corporation, China (LSYC201805), and the Hongyunhonghe Tobacco (Group) Co., Ltd., China (HYHH2016YL02).
Corresponding Authors:  Correspondence SONG Wen-jing, Tel/Fax: +86-532-66715918, E-mail: songwenjing@caas.cn; LIANG Hong-bo, E-mail: lianghongbo@caas.cn   
About author:  MENG Lin, E-mail: mlbio@126.com; DONG Jian-xin, E-mail:dongjiaxin@caas.cn; * These authors contributed equally to this study.

Cite this article: 

MENG Lin, DONG Jian-xin, WANG Shu-sheng, SONG Ke, LING Ai-fen, YANG Jin-guang, XIAO Zhi-xin, LI Wei, SONG Wen-jing, LIANG Hong-bo. 2019. Differential responses of root growth to nutrition with different ammonium/nitrate ratios involve auxin distribution in two tobacco cultivars. Journal of Integrative Agriculture, 18(12): 2703-2715.

Bennett A C, Adams F. 1970. Concentration of NH3 (aq) required for incipient NH3 toxicity to seedlings. Soil Science Society of America Journal, 34, 259–263.
Blakeslee J J, Peer W A, Murphy A S. 2005. Auxin transport. Current Opinion in Plant Biology, 8, 494–500.
Britto D T, Kronzucker H J. 2002. NH4+ toxicity in higher plants: A critical review. Journal of Plant Physiology, 159, 567–584.
Casimiro I, Marchant A, Bhalerao R, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero P J, Bennett M. 2001. Auxin transport promotes Arabidopsis lateral root initiation. The Plant Cell, 13, 843–852.
Cao Y W, Glass A D M, Crawford N M. 1993. Ammonium inhibition of Arabidopsis root-growth can be reversed by potassium and by auxin resistance mutations aux1, axr1, and axr2. Plant Physiology, 102, 983–989.
Chaillou S, Rideout J W, Raper C D, Morotgaudry J F. 1994. Responses of soybean to ammonium and nitrate supplied in combination to the whole root-system or separately in a split-root system. Physiologia Plantarum, 90, 259–268.
Chen Y N, Fan X R, Song W J, Zhang Y L, Xu G H. 2012. Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnology Journal, 10, 139–149.
Claussen W, Lenz F. 1995. Effect of ammonium and nitrate on net photosynthesis, flower formation, growth and yield of eggplants (Solanum melongena L.). Plant and Soil, 171, 267–274.
Cox W J, Reisenauer H M. 1973. Growth and ion uptake by wheat supplied nitrogen as nitrate, or ammonium, or both. Plant and Soil, 38, 363–380.
Drew M C. 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, Ashley T W. 1973. Nutrient supply and the growth of the seminal root system in barley. Journal of Experimental Botany, 24, 1189–1202.
Evans R D, Bloom A J, Sukrapanna S S, Ehleringer J R. 1996. Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition. Plant Cell and Environment, 19, 1317–1323.
Friml J. 2003. Auxin transport-shaping the plant. Current Opinion in Plant Biology, 6, 7–12.
Glass A D, Britto D T, Kaiser B N, Kinghorn J R, Kronzucker H J, Kumar A, Okamoto M, Rawat S, Siddiqi M Y, Unkles S E, Vidmar J J. 2002. The regulation of nitrate and ammonium transport systems in plants. Journal of Experimental Botany, 53, 855–864.
Granato T C, Raper J R. 1989. Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. Journal of Experimental Botany, 40, 263–275.
Guo S, Zhou Y, Shen Q, Zhang F. 2007. Effect of ammonium and nitrate nutrition on some physiological processes in higher plants - Growth, photosynthesis, photorespiration, and water relations. Plant Biology, 9, 21–29.
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 Science, 169, 894–900.
Hackett C. 1972. A method of applying nutrients locally to roots under controlled conditions, and some morphological effects of locally applied nitrate on the branching of wheat roots. Australian Journal of Biological Sciences, 25, 1169–1180.
Hoagland D R, Arnon D I. 1950. The water-culture method for growing plants without soil. Circular California Agricultural Experiment Station, 347, 357–359.
Hochholdinger F, Park W J, Sauer M, Woll K. 2004. From weeds to crops: Genetic analysis of root development in cereals. Trends in Plant Science, 9, 42–48.
Jiang F, Li C J, Jeschke W D, Zhang F S. 2001. Effect of top excision and replacement by 1-naphthylacetic acid on partition and flow of potassium in tobacco plants. Journal of Experimental Botany, 52, 2143–2150.
Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L. 2013. Lateral root development in Arabidopsis: Fifty shades of auxin. Trends in Plant Science, 18, 450–458.
Leyser O, Fitter A. 1998. Roots are branching out in patches. Trends in Plant Science, 3, 203–204.
Li Q, Li B H, Kronzucker H J, Shi W M. 2010. Root growth inhibition by NH4+ in Arabidopsis is mediated by the root tip and is linked to NH4+ efflux and GMPase activity. Plant Cell and Environment, 33, 1529–1542.
Linkohr B I, Williamson L C, Fitter A H, Leyser H M C. 2002. Nitrate and phosphate availability and distribution have different effects on root system of architecture of Arabidopsis. The Plant Journal, 29, 751–760.
Liu N, Zhang L, Meng X X, Neelam A, Yang J H, Zhang M F. 2014. Effect of nitrate/ammonium ratios on growth, root morphology and nutrient elements uptake of watermelon (Citrullus lanatus) seedlings. Journal of Plant Nutrition, 37, 1859–1872.
Ljung K, Bhalerao R P, Sandberg G. 2001. Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. The Plant Journal, 28, 465–474.
Lu Y L, Xu Y C, Shen Q R, Dong C X. 2009. Effects of different nitrogen forms on the growth and cytokinin content in xylem sap of tomato (Lycopersicon esculentum Mill.) seedlings. Plant and Soil, 315, 67–77.
Malamy J E, Ryan K S. 2001. Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiology, 127, 899–909.
Marschner H. 2012. Mineral nutrition of higher plants. Journal of Ecology, 76, 1250–1251.
Meng L, Song W J, Liu S J, Dong J X, Zhang Y L, Wang C D, Xu Y M, Wang S S. 2015. Light quality regulates lateral root development in tobacco seedlings by shifting auxin distributions. Journal of Plant Growth Regulation, 34, 574–583.
Peltier G, Thibault P. 1983. Ammonia exchange and photo-respiration in chlamydomonas. Plant Physiology, 71, 888–892.
Peret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, James N, Casimiro I, Perry P, Syed A. 2012. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. The Plant Cell, 24, 2874–2885.
Qian X Q, Shen Q R, Xu G H, Wang J, Zhou M Y. 2004. Nitrogen form effects on yield and nitrogen uptake of rice crop grown in aerobic soil. Journal of Plant Nutrition, 27, 1061–1076.
Raven J A, Wollenweber B, Handley L L. 1992. A comparison of ammonium and nitrate as nitrogen-sources for photolithotrophs. New Phytologist, 121, 19–32.
Reed R C, Brady S R, Muday G K. 1998. Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiology, 118, 1369–1378.
Robinson D. 1994. The responses of plants to non-uniform supplies of nutrients. New Phytologist, 127, 635–674.
Sattelmacher B, Gerendas J, Thoms K, Brück H, Bagdady N H. 1993. Interaction between root growth and mineral nutrition. Environmental and Experimental Botany, 33, 63–73.
Schmidt G W, Delaney S K. 2010. Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Molecular Genetics and Genomics, 283, 233–241.
Serna M D, Borras R, Legaz F, Primomillo E. 1992. The influence of nitrogen concentration and ammonium-nitrate ratio on N-uptake, mineral-composition and yield of citrus. Plant and Soil, 147, 13–23.
Song W J, Liu S J, Meng L, Xue R, Wang C D, Liu G L, Dong C X, Wang S S, Dong J X, Zhang Y L. 2015. Potassium deficiency inhibits lateral root development in tobacco seedlings by changing auxin distribution. Plant and Soil, 396, 163–173.
Song W J, Sun H, Li J, Gong X P, Huang S J, Zhu X, Zhang Y L, Xu G H. 2013. Auxin distribution is differentially affected by nitrate in roots of two rice cultivars differing in responsiveness to nitrogen. Annals of Botany, 112, 1383–1393.
Stitt M, Feil R. 1999. Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: Consequences for the regulation of biomass partitioning between shoots and root. Plant and Soil, 215, 143–153.
Tao L Z, Cheung A Y, Wu H M. 2002. Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. The Plant Cell, 14, 2745–2760.
Thomson K S, Hertel R,  Müller S, Tavares J E. 1973. 1-N-naphthylphthalamic acid and 2,3,5-triiodobenzoic acid. Planta, 109, 337–352.
Tian Q, Chen F, Zhang F, Mi G. 2005. Possible involvement of cytokinin in nitrate-mediated root growth in maize. Plant and Soil, 77, 185–196.
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 is correlated with reduced IAA levels in roots. Journal of Plant Physiology, 165, 942–951.
Ulmasov T, Murfett J, Hagen G, Guilfoyle T J. 1997. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. The Plant Cell, 9, 1963–1971.
Uysal A, Kuru B. 2013. Magnesium ammonium phosphate production from wastewater through box-behnken design and its effect on nutrient element uptake in plants. Clean-Soil Air Water, 41, 447–454.
Vanneste S, Friml J. 2009. Auxin: A trigger for change in plant development. Cell, 136, 1005–1016.
Vidal E A, Gutierrez R A. 2008. A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Current Opinion in Plant Biology, 11, 521–529.
Walch-Liu P, Neumann G, Bangerth F, Engels C. 2000. Rapid effects of nitrogen form on leaf morphogenesis in tobacco. Journal of Experimental Botany, 51, 227–237.
Wisniewska J, Xu J, Seifertova D, Brewer P B, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J. 2006. Polar PIN localization directs auxin flow in plants. Science, 312, 883–883.
Wiesler F. 1997. Agronomical and physiological aspects of ammonium and nitrate nutrition of plants. Journal of Plant Nutrition and Soil Science, 160, 227–238.
Wiersum L K. 1958. Density of root branching as affected by substrate and separate ions. Acta Botanica Neerlandica, 7, 174–190.
You W Q, Barker A V. 2004. Ethylene evolution and ammonium accumulation by tomato plants after root-applied glufosinate-ammonium treatment in the presence of ethylene inhibitors. Communications in Soil Science and Plant Analysis, 35, 1957–1965.
Zazimalova E, Murphy A S, Yang H, Hoyerova K, Hosek P. 2010. Auxin transporters - Why so many? Cold Spring Harbor Perspectives in Biology, 2, a001552.
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 H M, Rong H L, Pilbeam D. 2007. Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. Journal of Experimental Botany, 58, 2329–2338.
Zhang N G, Hasenstein K H. 1999. Initiation and elongation of lateral roots in Lactuca sativa. International Journal of Plant Sciences, 160, 511–519.
Zou C Q, Wang X F, Wang Z Y, Zhang F S. 2005. Potassium and nitrogen distribution pattern and growth of flue-cured tobacco seedlings influenced by nitrogen form and calcium carbonate in hydroponic culture. Journal of Plant Nutrition, 28, 2145–2157.
[1] LIU Yan, WANG Wei-ping, ZHANG Lin, ZHU Long-fu, ZHANG Xian-long, HE Xin. The HD-Zip transcription factor GhHB12 represses plant height by regulating the auxin signaling in cotton[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2015-2024.
[2] HOU Qian-dong, HONG Yi, WEN Zhuang, SHANG Chun-qiong, LI Zheng-chun, CAI Xiao-wei, QIAO Guang, WEN Xiao-peng. Molecular characterization of the SAUR gene family in sweet cherry and functional analysis of PavSAUR55 in the process of abscission[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1720-1739.
[3] CHEN Hong-yan, ZHU Zhu, WANG Xiao-wen, LI Yang-yang, HU Dan-ling, ZHANG Xue-fei, JIA Lu-qi, CUI Zhi-bo, SANG Xian-chun. Less hairy leaf 1, an RNaseH-like protein, regulates trichome formation in rice through auxin[J]. >Journal of Integrative Agriculture, 2023, 22(1): 31-40.
[4] LI Fu, YAN Dong, GAO Li-feng, LIU Pan, ZHAO Guang-yao, JIA Ji-zeng, REN Zheng-long. TaIAA15 genes regulate plant architecture in wheat[J]. >Journal of Integrative Agriculture, 2022, 21(5): 1243-1252.
[5] LIU Cong, LI De-xiong, HUANG Xian-biao, Zhang Fu-qiong, Xie Zong-zhou, Zhang Hong-yan, Liu Ji-hong. Manual thinning increases fruit size and sugar content of Citrus reticulata Blanco and affects hormone synthesis and sugar transporter activity[J]. >Journal of Integrative Agriculture, 2022, 21(3): 725-735.
[6] CHEN Juan-ni, WU Lin-tong, SONG Kun, ZHU Yun-song, DING Wei. Nonphytotoxic copper oxide nanoparticles are powerful “nanoweapons” that trigger resistance in tobacco against the soil-borne fungal pathogen Phytophthora nicotianae[J]. >Journal of Integrative Agriculture, 2022, 21(11): 3245-3262.
[7] JIANG Zhen-feng, LIU Dan-dan, WANG Tian-qiong, LIANG Xi-long, CUI Yu-hai, LIU Zhi-hua, LI Wen-bin. Concentration difference of auxin involved in stem development in soybean[J]. >Journal of Integrative Agriculture, 2020, 19(4): 953-964.
[8] LI Xiang, ZHANG Xiu-ge, XIAO Chun, GAO Yu-lin, DONG Wen-xia.
Behavioral responses of potato tuber moth (Phthorimaea operculella) to tobacco plant volatiles
[J]. >Journal of Integrative Agriculture, 2020, 19(2): 325-332.
[9] MA Ni, WAN Lin, ZHAO Wei, LIU Hong-fang, LI Jun, ZHANG Chun-lei.
Exogenous strigolactones promote lateral root growth by reducing the endogenous auxin level in rapeseed
[J]. >Journal of Integrative Agriculture, 2020, 19(2): 465-482.
[10] CAO Yuan-yuan, NI Hai-ting, LI Ting, LAY Khien-duc, LIU Dai-song, HE Xiang-yi, OU Kang-miao, TANG Xin-yun, WANG Xiao-bo, Qiu Li-juan. Pseudomonas sp. TK35-L enhances tobacco root development and growth by inducing HRGPnt3 expression in plant lateral root formation[J]. >Journal of Integrative Agriculture, 2020, 19(10): 2549-2560.
[11] WANG Shao-xi, SHI Feng-yan, DONG Xiang-xiang, LI Yu-xiang, ZHANG Zhi-hong, LI He. Genome-wide identification and expression analysis of auxin response factor (ARF) gene family in strawberry (Fragaria vesca)[J]. >Journal of Integrative Agriculture, 2019, 18(7): 1587-1603.
[12] TIAN Zhong-ling, SHI Hong-li, Munawar Maria, ZHENG Jing-wu. Pectate lyase is a factor in the adaptability for Heterodera glycines infecting tobacco[J]. >Journal of Integrative Agriculture, 2019, 18(3): 618-626.
[13] LIN Ying-chao, WEI Ke-su, GAO Wei-chang, CHEN Yi, LIN Ye-chun, CHEN Wei, LI Hong-xun, PAN Wen-jie. Effects of plastic mulching film-induced leaf burning on seedling growth in tobacco cultivation: Different findings beyond conservation view[J]. >Journal of Integrative Agriculture, 2018, 17(06): 1327-1337.
[14] LI Jun-xing, RAO Lin-li, XIE Hui, Monika Schreiner, CHEN Li-ping, LIU Yin-quan. Morphology and glucosinolate profiles of chimeric Brassica and the responses of Bemisia tabaci in host selection, oviposition and development[J]. >Journal of Integrative Agriculture, 2017, 16(09): 2009-2018.
[15] XU Yuan-yuan, WANG Jing, NIE Shan-shan, HUANG Dan-qiong, WANG Yan, XU Liang, WANG Rong-hua, LUO Xiao-bo, LIU Li-wang. Isolation and molecular characterization of the FLOWERING LOCUS C gene promoter sequence in radish (Raphanus sativus L.)[J]. >Journal of Integrative Agriculture, 2016, 15(4): 763-774.
No Suggested Reading articles found!