Abstract
Nitrogen is not only an essential nutrient for plant, but also an important signal molecule to integrate and regulate gene expression, metabolism and growth. Plant peptides are considered as a new type of hormone, and play an important regulatory role in plant growth and development. However, little is known about the co-regulation network between nitrogen and peptide hormones in plant. Here we identified an apple MdCLE8 gene, which encodes a putative peptide, induced by nitrogen deficiency in apple. Ectopic expression of MdCLE8 inhibited lateral root formation in Arabidopsis under nitrogen deficiency. Similarly, overexpression of MdCLE8 inhibited lateral root development in apple adventitious roots, and this inhibition was amplified under nitrogen deficiency treatment. Further studies showed that MdCLE8 may inhibit the expression of several key genes during lateral root emergence stage in Arabidopsis, thereby inhibiting the emergence of lateral root from root cortex cells. Collectively, our study not only broadened the gene regulatory network under the influence of nitrogen in apple, but also expanded the function of CLE peptide hormones in apple.
Key message
The apple peptide encoding gene MdCLE8 is induced by nitrogen deficiency signaling and negatively regulates lateral root formation in plants.
Data availability
All data generated or analysed during this study are included in this published article [and its supplementary information files].
References
An JP, Wang XF, Espley RV et al (2020) An apple b-box protein MdBBX37 modulates anthocyanin biosynthesis and hypocotyl elongation synergistically with MdMYBs and MdHY5. Plant Cell Physiol 61:130–143
Araya T, Miyamoto M, Wibowo J et al (2014a) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci USA 111:2029–2034
Araya T, Von Wirén N, Takahashi H (2014) CLE peptides regulate lateral root development in response to nitrogen nutritional status of plants. Plant Signal Behav 9:e29302
Atkinson RG, Johnston SL, Yauk YK et al (2009) Analysis of xyloglucan endotransglucosylase/hydrolase (XTH) gene families in kiwifruit and apple. Postharvest Biol Technol 51:149–157
Cai S, Lashbrook CC (2008) Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: Enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis Zinc Finger Protein2. Plant Physiol 146:1305–1321
Casimiro I, Marchant A, Bhalerao RP et al (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852
Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Cock JM, McCormick S (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol 126:939–942
Czyzewicz N, Yue K, Beeckman T, De Smet I (2013) Message in a bottle: Small signalling peptide outputs during growth and development. J Exp Bot 64:5281–5296
Dubrovsky JG, Rost TL, Colón-Carmona A, Doerner P (2001) Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214:30–36
Fletcher JC (2020) Recent advances in Arabidopsis CLE peptide signaling. Trends Plant Sci 25:1005–1016
Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914
Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68
Gancheva MS, Malovichko YV, Poliushkevich LO et al (2019) Plant peptide hormones. Russ J Plant Physiol 66:171–189
Giehl RFH, Gruber BD, von Wirén N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778
Goad DM, Zhu C, Kellogg EA (2017) Comprehensive identification and clustering of CLV3/ESR-related (CLE) genes in plants finds groups with potentially shared function. New Phytol 216:605–616
González-Carranza ZH, Elliott KA, Roberts JA (2007) Expression of polygalacturonases and evidence to support their role during cell separation processes in Arabidopsis thaliana. J Exp Bot 58:3719–3730
Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179
Hanada K, Zhang X, Borevitz JO et al (2007) A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res 17:632–640
Hanada K, Higuchi-Takeuchi M, Okamoto M et al (2013) Small open reading frames associated with morphogenesis are hidden in plant genomes. Proc Natl Acad Sci U S A 110:2395–2400
Hobe M, Müller R, Grünewald M et al (2003) Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol 213:371–381
Kinoshita A, Nakamura Y, Sasaki E et al (2007) Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-Related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48:1821–1825
Kumpf RP, Shi CL, Larrieu A et al (2013) Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proc Natl Acad Sci USA 110:5235–5240
Laskowski M, Biller S, Stanley K et al (2006) Expression profiling of auxin-treated Arabidopsis roots: Toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47:788–792
Lewis DR, Olex AL, Lundy SR et al (2013) A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell 25:3329–3346
Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell Environ 28:67–77
Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44
Meng D, Yang Q, Dong B et al (2019) Development of an efficient root transgenic system for pigeon pea and its application to other important economically plants. Plant Biotechnol J 17:1804–1813
Motomitsu A, Sawa S, Ishida T (2015) Plant peptide hormone signalling. Essays Biochem 58:115–131
Murphy E, Smith S, De Smet I (2012) Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198–3217
Ogawa M, Kay P, Wilson S, Swain SM (2009) Arabidopsis dehiscence zone polygalacturonase1 (ADPG1), ADPG2, and Quartet2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21:216–233
Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113
Péret B, De Rybel B, Casimiro I et al (2009a) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408
Péret B, Larrieu A, Bennett MJ (2009b) Lateral root emergence: a difficult birth. J Exp Bot 60:3637–3643
Remans T, Nacry P, Pervent M et al (2006a) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211
Remans T, Nacry P, Pervent M et al (2006b) A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol 140:909–921
Ruffel S, Krouk G, Ristova D et al (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci USA 108:18524–18529
Santiago J, Brandt B, Wildhagen M et al (2016) Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. Elife 5:e15075
Shajahan A, Thilip C, Faizal K et al (2017) An efficient hairy root system for withanolide production in Withania somnifera (L.) Dunal. Prod Plant Deriv Nat Compd through Hairy Root Cult 133–143.
Sung KC, Larue CT, Chevalier D et al (2008) Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:15629–15634
Swarup K, Benková E, Swarup R et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954
Takatsuka H, Umeda M (2014) Hormonal control of cell division and elongation along differentiation trajectories in roots. J Exp Bot 65:2633–2643
Tian D, Liu Y, Tian L et al (2019) Involvement of Populus CLEL peptides in root development. Tree Physiol 39:1907–1921
Vidal EA, Tamayo KP, Gutierrez RA (2010) Gene networks for nitrogen sensing, signaling, and response in Arabidopsis thaliana. Syst Biol Med 2:683–693
Vidal EA, Moyano TC, Riveras E et al (2013) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proc Natl Acad Sci USA 110:12840–12845
Vilches-Barro A, Maizel A (2015) Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Biol 23:31–38
Whitford R, Fernandez A, De Groodt R et al (2008) Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc Natl Acad Sci USA 105:18625–18630
Xue R, Wu X, Wang Y et al (2017) Hairy root transgene expression analysis of a secretory peroxidase (PvPOX1) from common bean infected by Fusarium wilt. Plant Sci 260:1–7
Zhang TE, Li XM, Zhao Q et al (2021) Genome-wide identification and functional characterization of the MdCLE peptide family in apple (Malus × domestica). Hortic Plant J (Accept).
Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–410
Zhou LJ, Zhang CL, Zhang RF et al (2019) The SUMO E3 ligase MdSIZ1 targets MdbHLH104 to regulate plasma membrane H +-ATPase activity and iron homeostasis. Plant Physiol 179:88–106
Zhu Q, Shao Y, Ge S et al (2019) A MAPK cascade downstream of IDA–HAE/HSL2 ligand–receptor pair in lateral root emergence. Nat Plants 5:414–423
Acknowledgements
This work was supported by National Key R&D Program of China (2018YFD1000100); National Natural Science Foundation of China (31772288); Natural Science Foundation of Shandong Province (ZR2020ZD43); Ministry of Agriculture of China (CARS-27).
Author information
Authors and Affiliations
Contributions
C-XY, QZ, and T-EZ conceived and designed the experiments. C-XY and QZ supervised the experiments. T-EZ, YS and X-ML performed the experiments. All the authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. The authors have no conflict of interest to declare.
Additional information
Communicated by Francisco de Assis Alves Mourão Filho.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, Te., Shi, Y., Li, Xm. et al. A peptide encoding gene MdCLE8 regulates lateral root development in apple. Plant Cell Tiss Organ Cult 148, 419–427 (2022). https://doi.org/10.1007/s11240-021-02182-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-021-02182-4