Roles and mechanisms of Ca²⁺ in regulating primary root growth of plants

References

• Petricka JJ, Winter CM, Benfey PN. Control of Arabidopsis root development. Ann Rev Plant Biol. 2012;63:1–6.
   PubMed Web of Science ®Google Scholar
• Motte H, Vanneste S, Beeckman T. Molecular and environmental regulation of root development. Ann Rev Plant Biol. 2019;70:465–488.
   PubMed Web of Science ®Google Scholar
• Waidmann S, Sarkel E, Kleine-Vehn J. Same same, but different: growth responses of primary and lateral roots. J Exp Bot. 2020. doi:10.1093/jxb/eraa027.
   PubMedGoogle Scholar
• Pacifici E, Polverari L, Sabatini S. Plant hormone cross-talk: the pivot of root growth. J Exp Bot. 2015;66:1113–1121.
   PubMed Web of Science ®Google Scholar
• Zhang J, Vanneste S, Brewer PB, Michniewicz M, Grones P, Kleine-Vehn J, Löfke C, Teichmann T, Bielach A, Cannoot B, et al. Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev Cell. 2011;20:855–866.
   PubMed Web of Science ®Google Scholar
• Vanneste S, Friml J. Calcium: the missing link in auxin action. Plants. 2013;2:650–675.
   Google Scholar
• Tsukagoshi H. Control of root growth and development by reactive oxygen species. Curr Opin Plant Biol. 2016;29:57–63.
   PubMed Web of Science ®Google Scholar
• Prakash V, Vishwakarma K, Singh VP, Rai P, Ramawat N, Tripathi KD, Sharma S. NO and ROS implications in organization of root system architecture. Plant Cell Environ. 2019. doi:10.1111/ppl.13050.
   Google Scholar
• Kudla J, Becker D, Grill E, Hedrich R, Hippler M, Kummer U, Parniske M, Romeis T, Schumacher K. Advances and current challenges in calcium signaling. New Phytol. 2018;218:414–431.
   PubMed Web of Science ®Google Scholar
• Liu J, Niu Y, Zhang J, Zhou Y, Ma Z, Huang X. Ca2+ channels and Ca2+ signals involved in abiotic stress responses in plant cells: recent advances. Plant Cell Tissue Organ Cult. 2018;132:413–424.
   Web of Science ®Google Scholar
• Thor K. Calcium—nutrient and messenger. Front Plant Sci. 2019;10:440.
   PubMed Web of Science ®Google Scholar
• Medvedev SS. Principles of calcium signal generation and transduction in plant cells. Russ J Plant Physl+. 2018;65:771–783.
   Web of Science ®Google Scholar
• Jiao YH, Sun LR, Song YL, Wang LM, Liu LP, Zhang LY, Liu B, Li N, Miao C, Hao FS. AtrbohD and AtrbohF positively regulate abscisic acid inhibited primary root growth by affecting Ca2+ signaling and auxin response of roots in Arabidopsis. J Exp Bot. 2013;64:4183–4192.
   PubMed Web of Science ®Google Scholar
• Chakraborty S, Toyota M, Moeder W, Chin K, Fortuna A, Champigny M, Vanneste S, Gilroy S, Beeckman T, Yoshioka K. A novel role for cyclic nucleotide-gated ion channel 2 (DND1) in auxin signaling. BioRxiv. 2018. doi:10.1101/508572.
   Google Scholar
• Hazak O, Mamon E, Lavy M, Sternberg H, Behera S, Schmitz-Thom I, Bloch D, Dementiev O, Gutman I, Danziger T, et al. A novel Ca2+-binding protein that can rapidly transduce auxin responses during root growth. PLoS Biol. 2019;17(7):e3000085.
   PubMed Web of Science ®Google Scholar
• Leitão N, Dangeville P, Carter R, Charpentier M. Nuclear calcium signatures are associated with root development. Nat Commun. 2019;10:4865.
   PubMed Web of Science ®Google Scholar
• Meena MK, Vishwakarma NK, Tripathi V, Chattopadhyay D. CBL-interacting protein kinase 25 contributes to root meristem development. J Exp Bot. 2019;70:133–147.
   PubMed Web of Science ®Google Scholar
• Goh CS, Lee Y, Kim S-H. Calcium could be involved in auxin-regulated maintenance of the quiescent center in the Arabidopsis root. J Plant Biol. 2012;55:143–150.
   Web of Science ®Google Scholar
• Leyser O. Auxin signaling. Plant Physiol. 2018;176:465–479.
   PubMed Web of Science ®Google Scholar
• Gallei M, Luschnig C, Friml J. Auxin signalling in growth: schrodinger’s cat out of the bag. Curr Opin Plant Biol. 2019;53:43–49.
   PubMed Web of Science ®Google Scholar
• Lu TT, Zhang GF, Sun LR, Wang J, Hao FS. Genome-wide identification of CBL family and expression analysis of CBLs in response to potassium deficiency in cotton. PeerJ. 2017;5:e3653.
   PubMed Web of Science ®Google Scholar
• Meena MK, Ghawana S, Dwivedi V, Roy A, Chattopadhyay D. Expression of chickpea CIPK25 enhances root growth and tolerance to dehydration and salt stress in transgenic tobacco. Front Plant Sci. 2015;6:683.
   PubMed Web of Science ®Google Scholar
• Li P, Zhao C, Zhang Y, Wang X, Wang X, Wang J, Wang F, Bi Y. Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis in Arabidopsis seedlings. Protoplasma. 2016;253:185–200.
   PubMed Web of Science ®Google Scholar
• Fasani E, DalCorso G, Costa A, Zenoni S, Furini A. The Arabidopsis thaliana transcription factor MYB59 regulates calcium signalling during plant growth and stress response. Plant Mol Biol. 2019;99:517–534.
   PubMed Web of Science ®Google Scholar
• Teaster ND, Sparks JA, Blancaflor EB, Hoagland RE. Interactions of auxinic compounds on a Ca2+ signaling and root growth in Arabidopsis thaliana. Am J Plant Sci. 2015;6:2989–3000.
   Google Scholar
• Wybouw B, Rybel B. Cytokinin – a developing story. Trends Plant Sci. 2019;24:177–185.
   PubMed Web of Science ®Google Scholar
• Liu J, Moore S, Chen C, Lindsey K. Crosstalk complexities between auxin, cytokinin, and ethylene in Arabidopsis root development: from experiments to systems modeling, and back again. Mol Plant. 2017;10:1480–1496.
   PubMed Web of Science ®Google Scholar
• Di Mambro R, De Ruvo M, Pacifici E, Salvi E, Sozzani R, Benfey PN, Busch W, Novak O, Ljung K, Di Paola L, et al. Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proc Natl Acad Sci USA. 2017;114:7641–7649.
   PubMed Web of Science ®Google Scholar
• Wei Z, Li J. Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant. 2016;9:86–100.
   PubMed Web of Science ®Google Scholar
• Bergonci T, Ribeiro B, Ceciliato PHO, Guerrero-Abad JC, Silva-Filho MC, Moura DS. Arabidopsis thaliana RALF1 opposes brassinosteroid effects on root cell elongation and lateral root formation. J Exp Bot. 2014;65:2219–2230.
   PubMed Web of Science ®Google Scholar
• Campos WF, Dressano K, Ceciliato PHO, Guerrero-Abad JC, Silva AL, Fiori CS, Morato Do Canto A, Bergonci T, Claus LAN, Silva-Filho MC, et al. Arabidopsis thaliana rapid alkalinization factor 1-mediated root growth inhibition is dependent on calmodulin-like protein 38. J Biol Chem. 2018;293:2159–2171.
   PubMed Web of Science ®Google Scholar
• Matos JL, Fiori CS, Silva-Filho MC, Moura DS. A conserved dibasic site is essential for correct processing of the peptide hormone AtRALF1 in Arabidopsis thaliana. FEBS Lett. 2008;582:3343–3347.
   PubMed Web of Science ®Google Scholar
• Song Y, Miao Y, Song CP. Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol. 2014;201:1121–1140.
   PubMed Web of Science ®Google Scholar
• Chan Z, Yokawa K, Kim WY, Song CP. ROS regulation during plant abiotic stress responses. Front Plant Sci. 2016;7:1536.
   PubMed Web of Science ®Google Scholar
• Mhamdi A, Breusegem FV. Reactive oxygen species in plant development. Development. 2018;145:dev164376.
   PubMed Web of Science ®Google Scholar
• Qi J, Song CP, Wang B, Zhou J, Kangasjärvi J, Zhu JK, Gong Z. Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J Integr Plant Biol. 2018;60:67–88.
   Web of Science ®Google Scholar
• Ma X, Zhang X, Yang L, Tang M, Wang K, Wang L, Bai L, Song CP. Hydrogen peroxide plays an important role in PERK4-mediated abscisic acid-regulated root growth in Arabidopsis. Funct Plant Biol. 2018;46:165–174.
   Web of Science ®Google Scholar
• Sun LR, Zhao ZJ, Hao FS. NADPH oxidases, essential players of hormone signalings in plant development and response to stresses. Plant Signal Behav. 2019;14:e1657343.
   PubMed Web of Science ®Google Scholar
• Lee Y. Redox control on stem cell fate and maintenance in the root. J Plant Biol. 2019;62:320–328.
   Web of Science ®Google Scholar
• Zhang G, Yue C, Lu T, Sun L, Hao F. Genome-wide identification and expression analysis of NADPH oxidase genes in response to ABA and abiotic stresses, and in fibre formation in Gossypium. PeerJ. 2020;8:e8404.
   PubMed Web of Science ®Google Scholar
• Ma LY, Zhang H, Sun LR, Jiao YH, Zhang GZ, Miao C, Hao FS. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot. 2012;63:305–317.
   PubMed Web of Science ®Google Scholar
• Liu B, Sun LR, Ma LY, Hao FS. Both AtrbohD and AtrbohF are essential for mediating responses to oxygen deficiency in Arabidopsis. Plant Cell Rep. 2017;36:947–957.
   PubMed Web of Science ®Google Scholar
• Sun LR, Ma LY, He SB, Hao FS. AtrbohD functions downstream of ROP2 and positively regulates waterlogging response. Plant Signal Behav. 2018;13:e1513300.
   PubMed Web of Science ®Google Scholar
• Chen Q, Yang G. Signal function studies of ROS, especially RBOH dependent ROS, in plant growth, development and environmental stress. J Plant Growth Regul. 2019. doi:10.1007/s00344-019-09971-4.
   PubMed Web of Science ®Google Scholar
• Li N, Sun LR, Zhang LY, Song YL, Hu PP, Li C, Hao FS. AtrbohD and AtrbohF negatively regulate lateral root development by changing the localized accumulation of superoxide in primary roots of Arabidopsis. Planta. 2015;241:591–602.
   PubMed Web of Science ®Google Scholar
• Demidchik V, Shabala S. Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ Hub’. Funct Plant Biol. 2017;45:9–27.
   Web of Science ®Google Scholar
• Chen K, Li G, Bressan RA, Song C, Zhu J, Zhao Y. Abscisic acid dynamics, signaling and functions in plants. J Integr Plant Biol. 2020;62:25–54.
   PubMed Web of Science ®Google Scholar
• Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. Embo J. 2003;22:2623–2633.
   PubMed Web of Science ®Google Scholar
• Han S, Fang L, Ren X, Wang W, Jiang J. MPK6 controls H2O2-induced root elongation by mediating Ca2+ influx across the plasma membrane of root cells in Arabidopsis seedlings. New Phytol. 2015;205:695–706.
   PubMed Web of Science ®Google Scholar
• Han JP, Koster P, Drerup MM, Scholz M, Li S, Edel KH, Hashimoto K, Kuchitsu K, Hippler M, Kudla J. Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca2+ binding. New Phytol. 2019;221:1935–1949.
   PubMed Web of Science ®Google Scholar
• Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulze WX, Romeis T. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci USA. 2013;110:8744–8749.
   PubMed Web of Science ®Google Scholar
• Drerup MM, Schl€ucking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J. The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant. 2013;6:559–569.
   PubMed Web of Science ®Google Scholar
• Qin H, He L, Huang R. The coordination of ethylene and other hormones in primary root development. Front Plant Sci. 2019;10:874.
   PubMed Web of Science ®Google Scholar
• Luo X, Chen Z, Gao J, Gong Z. Abscisic acid inhibits root growth in Arabidopsis through ethylene biosynthesis. Plant J. 2014;79:44–55.
   PubMed Web of Science ®Google Scholar
• Vaahtera L, Schulz J, Hamann T. Cell wall integrity maintenance during plant development and interaction with the environment. Nat Plants. 2019;5:924–932.
   PubMed Web of Science ®Google Scholar
• Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu M-C, Maman J, Steinhorst L, Schmitz-Thom I, et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol. 2018;28:666–675.e5.
   PubMed Web of Science ®Google Scholar
• Zhang J, Zhang X, Wang R, Li W. The plasma membrane-localised Ca2+-ATPase ACA8 plays a role in sucrose signalling involved in early seedling development in Arabidopsis. Plant Cell Rep. 2014. doi:10.1007/s00299-014-1590-y.
   Web of Science ®Google Scholar
• Singh SK, Chien CT, Chang IF. The Arabidopsis glutamate receptor-like gene GLR3.6 controls root development by repressing the Kip-related protein gene KRP4. J Exp Bot. 2016;67:1853–1869.
   PubMed Web of Science ®Google Scholar