Root hair specification and its growth in response to nutrients

Authors

  • Xian HUANG Yangtze University, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Jingzhou, Hubei 434020; Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Tianzhi GONG Yangtze University, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Jingzhou, Hubei 434020; Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Mei LI Yangtze University, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Jingzhou, Hubei 434020; Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Cenghong HU Yangtze University, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Jingzhou, Hubei 434020; Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Dejian ZHANG Yangtze University, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Jingzhou, Hubei 434020; Xinyang Agriculture and Forestry University, Henan Key Laboratory of Tea Plant Comprehensive Utilization in South Henan Xinyang, Henan 464000; Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Mufang SUN Xinyang Agriculture and Forestry University, Henan Key Laboratory of Tea Plant Comprehensive Utilization in South Henan Xinyang, Henan 464000; Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)

DOI:

https://doi.org/10.15835/nbha49212258

Keywords:

calcium, iron, magnesium, nitrogen, phosphorus, potassium, root hair, ROS

Abstract

Plant root hairs are cylindrical tubular projections from root epidermal cells. They increase the root surface area, which is important for the acquisition of water and nutrients, microbe interactions, and plant anchorage. The root hair specification, the effect of root hairs on nutrient acquisition and the mechanisms of nutrients (calcium, iron, magnesium, nitrogen, phosphorus, and potassium) that affect root hair development and growth were reviewed. The gene regulatory network on root hair specification in the plant kingdom was highlighted. More work is needed to clone the genes of additional root hair mutants and elucidate their roles, as well as undertaking reverse genetics and mutant complementation studies to add to the current knowledge of the signaling networks, which are involved in root hair development and growth regulated by nutrients.

References

Bates TR, Lynch JP (1996). Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell and Environment 19:529-538. https://doi.org/10.1111/j.1365-3040.1996.tb00386.x

Becker D, Stanke R, Fendrik I, Frommer WB, Vanderleyden J, … Hedrich R (2002). Expression of the NH4+-transporter gene LEAMT1;2 is induced in tomato roots upon association with N2-fixing bacteria. Planta 215:424-429. https://doi.org/10.1007/s00425-002-0773-x

Berger F, Haseloff J, Schiefelbein J, Dolan L (1998). Positional information in root epidermis is defined during embryogenesis and acts in domains with strict boundaries. Current Biology 8:421-430. https://doi.org/10.1016/s0960-9822(98)70176-9

Bhosale R, Giri J, Pandey BK, Giehl RFH, Hartmann A, … Swarup R (2018). A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nature Communications 9:1409. https://doi.org/10.1038/s41467-018-03851-3

Bibikova TN, Zhigilei A, Gilroy S (1997). Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495-505. https://doi.org/10.1007/s004250050219

Bloch D, Monshausen G, Gilroy S, Yalovsky S (2011). Co-regulation of root hair tip growth by ROP GTPases and nitrogen source modulated pH fluctuations. Plant Signaling and Behavior 6:426-429. https://doi.org/10.4161/psb.6.3.14523

Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, ... Schiefelbein J (2012). A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genetics 8:e1002446. https://doi.org/10.1371/journal.pgen.1002446

Cao X, Chen CL, Zhang DJ, Shu B, Xiao J, Xia RX (2013). Influence of nutrient deficiency on root architecture and root hair morphology of Trifoliata orange (Poncirus trifoliata L. Raf.) seedlings under sand culture. Scientia Horticulturae 162:100-105. https://doi.org/10.1016/j.scienta.2013.07.034

Carol RJ, Dolan L (2006). The role of reactive oxygen species in cell growth: lessons from root hairs. Journal Experimental Botany 57:1829-1834. https://doi.org/10.1093/jxb/erj201

Chen SY, Wang SC (2019). GLABRA2, A common regulator for epidermal cell fate determination and anthocyanin biosynthesis in Arabidopsis. International Journal of Molecular Sciences 20:4997. https://doi.org/10.3390/ijms20204997

Clowes FAL (2000). Pattern in root meristem development in angiosperms. New Phytologist 146:83-94. https://doi.org/10.1046/j.1469-8137.2000.00614.x

Curie C, Mari S (2017). New routes for plant iron mining. New Phytologist 214:521. https://doi.org/10.1111/nph.14364

Dolan L, Costa S (2001). Evolution and genetics of root hair stripes in the root epidermis. Journal Experimental Botany 52:413-417. https://doi.org/10.1093/jexbot/52.suppl_1.413

Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, … Dolan L (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-446. https://doi.org/10.1038/nature01485

Gahoonia TS, Nielsen NE (1998). Direct evidence on participation of root hair in phosphorus (32P) uptake from soil. Plant and Soil 198:147-152. https://www.jstor.org/stable/24122651

Gassmann W, Schroeder JI (1994). Inward-rectifying K+ channels in root hairs of wheat: A mechanism for aluminum-sensitivelow-affinity K+ uptake and membrane potential control. Plant Physiology 105:1399-1408. https://doi.org/10.1104/pp.105.4.1399

Gilroy S, Jones DL (2020). Through form to function: root hair development and nutrient uptake. Trends in Plant Science 5:56-60. https://doi.org/10.1016/s1360-1385(99)01551-4

Giri J, Bhosale R, Huang G, Pandey BK, Parker H, Bennett MJ (2018). Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nature Communications 9:1408. https://doi.org/10.1038/s41467-018-03850-4

Grierson CS, Parker JS, Kemp AC (2015). Arabidopsis genes with roles in root hair development. Journal of Plant Nutrition and Soil Science 164:131-140. http://dx.doi.org/10.1002/1522-2624(200104)164:2<131::AID-JPLN131>3.3.CO;2-2

Grierson C, Nielsen E, Ketelaar T, Schiefelbein J (2014). Root hairs. The Arabidopsis book, American Society of Plant Biologists 12:e0172. http://dx.doi.org/10.1199/tab.0060

Han GL, Wei XC, Dong XX, Wang CF, Sui N, … Wang BS (2020). Arabidopsis ZINC FINGER PROTEIN1 acts downstream of GL2 to repress root hair initiation and elongation by directly suppressing bHLH genes. The Plant Cell 32:206-225. https://doi.org/10.1105/tpc.19.00226

Hepler PK, Vidali L, Cheung AY (2001). Polarized cell growth in higher plants. Annual Review of Cell and Developmental Biology 17:159-187. https://doi.org/10.1146/annurev.cellbio.17.1.159

Huang C, Jiao X, Yang L, Yang L, Zhang M, … Song C (2019). ROP-GEF signal transduction is involved in AtCAP1-regulated root hair growth. Plant Growth Regulation 87:1-8. https://doi.org/10.1007/s10725-018-0448-7

Huang G, Liang W, Sturrock CJ, Pandey BK, Giri J, … Zhang D (2018). Rice actin binding protein RMD controls crown root angle in response to external phosphate. Nature Communications 9:2346. https://doi.org/10.1038/s41467-018-04710-x

Jung JY, Shin R, Schachtman DP (2009). Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. The Plant Cell 21: 607. https://doi.org/10.1105/tpc.108.063099

Jungk A (2001). Root hairs and the acquisition of plant nutrients from soil. Journal of Plant Nutrition and Soil Science 164:121-129. https://doi.org/10.1002/1522-2624(200104)164:23.0.CO;2-6

Kadota Y, Goh T, Tomatsu H, Tamauchi R, Higashi K ... Kuchitsu K (2004). Cryptogein-induced initial events in tobacco BY-2 cells:pharmacological characterization of molecular relationship among cytosolic Ca2+ transients, anion efflux and production of reactive oxygen species. Plant Cell and Physiology 45:160-170. https://doi.org/10.1093/pcp/pch020

Kang YH, Song SK, Schiefelbein J, Lee MM (2013). Nuclear trapping controls the position-dependent localization of CAPRICE in the root epidermis of Arabidopsis. Plant Physiology 163:193-204. https://doi.org/10.1104/pp.113.221028

Kim CM, Dolan L (2011). Root hair development involves asymmetric cell division in Brachypodium distachyon and symmetric division in Oryza sativa. New Phytologist 192:601-610. https://doi.org/10.1111/j.1469-8137.2011.03839.x

Kim DW, Lee SH, Choi SB, Won SK, Heo YK, … Cho HT (2006). Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. The Plant Cell 18:2958-2970. https://doi.org/10.1105/tpc.106.045229

Kirik V, Simon M, Huelskamp M, Schiefelbein J (2004). The enhancer of try and CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Developmental Biology 268:506-513. https://doi.org/10.1016/j.ydbio.2003.12.037

Kohli PS, Verma PK, Verma R, Parida SK, Giri J (2020). Genome-wide association study for phosphate deficiency responsive root hair elongation in chickpea. Functional & Integrative Genomics 20:1-12. https://doi.org/10.1007/s10142-020-00749-6

Kwak SH, Schiefelbein J (2014). TRIPTYCHON, not CAPRICE, participates in feedback regulation of SCM expression in the Arabidopsis root epidermis. Plant Signaling & Behavior 9:e973815. https://doi.org/10.4161/15592324.2014.973815

Kwak SH, Shen R, Schiefelbein J (2005). Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307:1111-1113. https://doi.org/10.1126/science.1105373

Kwak SH, Schiefelbein J (2008). A feedback mechanism controlling SCRAMBLED receptor accumulation and cell-type pattern in Arabidopsis. Current Biology 18:1949-1954. https://doi.org/10.1016/j.cub.2008.10.064

Lee MM, Schiefelbein J (1999). WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99:473-483. https://doi.org/10.1016/S0092-8674(00)81536-6

Li S, Yu JL, Zhu M, Zhao F, Luan S (2012). Cadmium impairs ion homeostasis by altering K+, and Ca2+, channel activities in rice root hair cells. Plant, Cell and Environment 35:1998-2013. https://doi.org/10.1111/j.1365-3040.2012.02532.x

Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010). Root hair systems biology. Trends in Plant Science 15:641-650. https://doi.org/10.1016/j.tplants.2010.08.010

Lin CY, Huang LY, Chi WC, Huang TL, Kakimoto T, … Huang HJ (2015). Pathways involved in vanadate-induced root hair formation in Arabidopsis. Physiologia Plantarum 153:137-148. https://doi.org/10.1111/ppl.12229

Liu CY, Zhang F, Zhang DJ, Zou YN, Shu B, Wu QS (2020). Transcriptome analysis reveals improved root hair growth in trifoliate orange seedlings by arbuscular mycorrhizal fungi. Plant Growth Regulation 92:195-203. https://doi.org/10.1007/s10725-020-00630-3

Long Y, Schiefelbein J (2020). Novel TTG1 mutants modify root-hair pattern formation in Arabidopsis. Frontiers in Plant Science 11:383. https://doi.org/10.3389/fpls.2020.00383

Macdonald GK, Bennett EM, Potter PA, Ramankutty N (2011). Agronomic phosphorus imbalances across the world’ s croplands. Proceedings of the National Academy of Sciences of the United States of America 108:3086-3091. https://doi.org/10.1073/pnas.1010808108

Miao BH, Han XG, Zhang WH (2010). The ameliorative effect of silicon on soybean seedlings grown in potassium-deficient medium. Annals of Botany 105:967-973. https://doi.org/10.1093/aob/mcq063

Muller M, Schmidt W (2004). Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiology 134:409-419. https://doi.org/10.1104/pp.103.029066

Narang RA, Bruene A, Altmann T (2000). Analysis of phosphate acquisition efficiency in different Arabidopsis accessions. Plant Physiology 124:1786-1799. https://doi.org/10.1104/pp.124.4.1786

Nestler J, Liu S, Wen TJ, Paschold A, Marcon C, … Hochholdinger F (2014). Roothairless5, which functions in maize (Zea mays L.) root hair initiation and elongation encodes a monocot-specific NADPH oxidase. The Plant Journal 79:729-740. https://doi.org/10.1111/tpj.12578

Niu Y, Jin G, Yong SZ (2014). Root development under control of magnesium availability. Plant Signaling & Behavior 9:e29720. https://doi.org/10.4161/psb.29720

Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann KA, … Hatzopoulos P (2001). TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. The Plant Cell 13:139-151. https://doi.org/10.1105/tpc.13.1.139

Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, … Hatzopoulos P (2013). Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytologist 197:1130-1141. https://doi.org/10.1111/nph.12092

Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016). The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848-1858. https://doi.org/10.1242/dev.132845

Savage N, Yang TJW, Chen CY, Lin KL, Monk NAM, Schmidt W (2013). Positional signaling and expression of ENHANCER OF TRY AND CPC1 are tuned to increase root hair density in response to phosphate deficiency in Arabidopsis thaliana. PLoS One 8:e75452. https://doi.org/10.1371/journal.pone.0075452

Schmidt W, Schikora A (2001). Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiology 125:2078-2084. https://doi.org/10.1104/pp.125.4.2078

Shaul O (2002). Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309-323. https://doi.org/10.1023/A:1016091118585

Shin R, Berg RH, Schachtman DP (2005). Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiology 46:1350-1357. https://doi.org/10.1093/pcp/pci145

Song SK, Ryu KH, Kang YH, Song JH, Cho YH, … Lee MM (2011). Cell fate in the Arabidopsis root epidermis is determined by competition between Werewolf and Caprice. Plant Physiology 157:1196-208. https://doi.org/10.1104/pp.111.185785

Sundaravelpandian K, Chandrika NNP, Schmidt W (2013). PFT1, a transcriptional Mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis. New Phytologist 197:151-161. https://doi.org/10.1111/nph.12000

Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008). Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241-1244. https://doi.org/10.1126/science.1152505

Hasanaklou HT, Ghadim AEK, Moradi F, Ghodehkahriz SJ, Gholipouri A (2020). The effects of NH4+ and NO3- and plant growth regulators on the accumulation of nutrients, carbohydrates and secondary metabolites of stevia rebaudiana bertoni. Sugar Tech 2020(2). https://doi.org/10.1007/s12355-020-00875-2

Tortosa M, Cartea ME, Velasco P, Soengas P, Rodriguez VM (2019). Calcium-signaling proteins mediate the plant transcriptomic response during a well-established Xanthomonas campestris pv. campestris infection. Horticulture Research 6:1-10. https://doi.org/10.1038/s41438-019-0186-7

Tsai HH, Schmidt W (2017). Mobilization of iron by plant-borne coumarins. Trends in Plant Science 22:538-548. https://doi.org/10.1016/j.tplants.2017.03.008

Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A (2004). Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. The Plant Journal 40:523-535. https://doi.org/10.1111/j.1365-313x.2004.02230.x

Wada T, Tachibana T, Shimura Y, Okada K (1997). Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113-1116. https://doi.org/10.1126/science.277.5329.1113

Wang W, Hui RK, Christa B, John S (2019). Root epidermal cell patterning is modulated by a critical residue in the WEREWOLF transcription factor. Plant Physiology 181:1239-1256. https://doi.org/10.1104/pp.19.00458

Wang Y, Kristian TK, Stoumann JL, Jakob M (2016). Vigorous root growth is a better indicator of early nutrient uptake than root hair traits in spring wheat grown under low fertility. Frontiers in Plant Science 7:865. https://doi.org/10.3389/fpls.2016.00865

Wang Y, Wu B, Berns AE, Xing Y, Amelung W (2020). Magnesium isotope fractionation reflects plant response to magnesium deficiency in magnesium uptake and allocation: a greenhouse study with wheat. Plant and Soil 455:93-105. https://doi.org/10.1007/s11104-020-04604-2

Westphal L, Strehmel N, Eschen-Lippold L, Bauer N, Westermann B, … Lee J (2019). pH effects on plant calcium fluxes: lessons from acidification-mediated calcium elevation induced by the γ-glutamyl-leucine dipeptide identified from Phytophthora infestans. Scientific Reports 9:4733. https://doi.org/10.1038/s41598-019-41276-0

Wymer CL, Bibikova TN, Gilroy S (1997). Cytoplasmic free calcium distribution during the development of root hairs of Arabidopsis thaliana. The Plant Journal 12:427-439. https://doi.org/10.1046/j.1365-313X.1997.12020427.x

Yang N, Zhu C, Gan L, Ng D, Xia K (2011). Ammonium-stimulated root hair branching is enhanced by methyl jasmonate and suppressed by ethylene in Arabidopsis thaliana. Journal of Plant Biology 54:92-100. https://doi.org/10.1007/s12374-011-9147-x

Yao H, Wang G, Guo L, Wang X (2013). Phosphatidic acid interacts with a MYB transcription factor and regulates its nuclear localization and function in Arabidopsis. The Plant Cell 25:5030-5042. https://doi.org/10.1105/tpc.113.120162

Yoshioka H, Sugie K, Park HJ, Maeda H, Doke N (2001). Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Molecular Plant Microbe Interactions 14:725-736. https://doi.org/10.1094/MPMI.2001.14.6.725

Zhang DJ, Xia RX, Cao X, Shu B, Chen CL (2013). Root hair development of Poncirus trifoliata grown in different growth cultures and treated with 3-indolebutyric acid and ethephon. Scientia Horticulturae 160:389-397. https://doi.org/10.1016/j.scienta.2013.06.007

Zhang YY, Zhu HY, Zhang Q, Li M, Wang X (2009). Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. The Plant Cell 21:2357-2377. https://doi.org/10.1105/tpc.108.062992

Zhu J, Kaeppler SM, Lynch JP (2005). Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant and Soil 270:299-310. https://doi.org/10.1007/s11104-004-1697-y

Downloads

Published

2021-06-14

How to Cite

HUANG, X. ., GONG, T., LI, M., HU, C. ., ZHANG, D., & SUN, M. (2021). Root hair specification and its growth in response to nutrients. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(2), 12258. https://doi.org/10.15835/nbha49212258

Issue

Section

Review Articles
CITATION
DOI: 10.15835/nbha49212258