SpringerLink
Log in

Enhanced root growth and nitric oxide content in ‘Mandarin’ lime under drought stress: experimental evidence

  • Biochemistry & Physiology - Short Communication
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Our aim was to test the hypothesis that root growth of ‘Mandarin’ lime—a drought tolerant citrus rootstock—under water deficit is associated with higher nitric oxide (NO) content in roots. As a reference, ‘Swingle’ citrumelo was compared with ‘Mandarin’ lime, two well-known citrus rootstocks. ‘Valencia’ sweet orange plants grafted on ‘Mandarin’ lime or ‘Swingle’ citrumelo were kept well-hydrated or grown under water withholding. After 14 days of water deficit, root morphology was evaluated, and leaf and root samples were collected for NO analysis. Under low water availability, ‘Mandarin’ lime exhibited higher root NO content and root growth than ‘Swingle’ citrumelo. Indeed, NO seems to modulate not only root biomass accumulation but also root morphology as higher NO was associated with large increase in root length and area. Such findings suggest that root NO content is a relevant marker for early screening of drought-tolerant citrus genotypes. As a novelty, we show that ‘Mandarin’ lime drought tolerance is significantly associated with root NO content.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Data availability

Data will be made available on request.

Abbreviations

ABA:

Abscisic acid

DAF2-DA:

4,5 Diaminofluorescein-2 diacetate

MWC:

Maximum water storage capacity

NO:

Nitric oxide

NOS:

Nitric oxide synthase

VPD:

Air vapor pressure deficit

WD:

Water deficit

References

  • Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411

    Article  CAS  PubMed  Google Scholar 

  • Bright J, Hiscock SJ, James PE, Hancock JT (2009) Pollen generates nitric oxide and nitrite: a possible link to pollen-induced allergic responses. Plant Physiol Biochem 47:49–55

    Article  CAS  PubMed  Google Scholar 

  • Castle WS, Baldwin JC, Muraro RP, Littell R (2010) Performance of ‘Valencia’ sweet orange trees on 12 rootstocks at two locations and an economic interpretation as a basis for rootstock selection. HortScience 45:523–533

    Article  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Lanteri ML, Garcia-Mata C, Have AT, Laxalt AM, Graziano M, Lamattina L (2007) Nitric oxide functions as intermediate in auxin, abscisic acid and lipid signaling pathways. In: Lamattina L, Polacco J (eds) Nitric oxide in plant growth, development and stress physiology, plant cell monographs. Springer, Berlin, pp 113–130

    Google Scholar 

  • Cuneo IF, Barrios-Masias F, Knipfer T, Uretsky J, Reyes C, Lenain P, Brodersen CR, Walker MA, McElrone AJ (2021) Differences in grapevine rootstock sensitivity and recovery from drought are linked to fine root cortical lacunae and root tip function. New Phytol 229:272–283

    Article  CAS  PubMed  Google Scholar 

  • Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520

    Article  CAS  PubMed  Google Scholar 

  • Foresi N, Mayta ML, Lodeyro AF, Scuffi D, Correa-Aragunde N, García-Mata C, Casalongué C, Carrillo N, Lamattina L (2015) Expression of the tetrahydrofolate-dependent nitric oxide synthase from the green alga Ostreococcus tauri increases tolerance to abiotic stresses and influences stomatal development in Arabidopsis. Plant J 82:806–821

    Article  CAS  PubMed  Google Scholar 

  • Gouvea C, Souza J, Magalhaes A, Martins I (1997) NO releasing substances that induce growth elongation in maize root segments. Plant Growth Regul 21:183–187

    Article  CAS  Google Scholar 

  • Hancock JT (2012) NO synthase in plants? Period. Biol 114:19–24

    Google Scholar 

  • Hancock JT, Neill SJ (2019) Nitric oxide: its generation and interactions with other reactive signaling compounds. Plants 8:41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma M, Wendehenne D, Philippot L, Hänsch R, Flemetakis E, Hu B, Rennenberg H (2020) Physiological significance of pedospheric nitric oxide for root growth, development and organismic interactions. Plant Cell Environ 43:2336–2354

    Article  CAS  PubMed  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari H-S, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518

    Article  PubMed  Google Scholar 

  • Medina CL, Machado EC (1998) Gas exchange and water relations of Valencia orange tree grafted on Rangpur lime and Poncirus trifoliata submitted to a water deficit. Bragantia 57:15–22

    Article  Google Scholar 

  • Medina CL, Machado EC, Pinto JM (1998) Fotossíntese de laranjeira “Valência” enxertada sobre quatro porta-enxertos e submetida à deficiência hídrica. Bragantia 57:1–14

    Article  Google Scholar 

  • Miranda MT, Silva SF, Moura BB, Hayashi AH, Machado EC, Ribeiro RV (2018) Hydraulic redistribution in Citrus rootstocks under drought. Theor Exp Plant Physiol 30:165–172

    Article  CAS  Google Scholar 

  • Miranda MT, Silva SF, Silveira NM, Pereira L, Machado EC, Ribeiro RV (2021) Root osmotic adjustment and stomatal control of leaf gas exchange are dependent on citrus rootstocks under water deficit. J Plant Growth Regul 40:11–19

    Article  CAS  Google Scholar 

  • Miranda MT, Espinoza-Núñez E, Silva SF, Pereira L, Hayashi AH, Boscariol-Camargo RL, Carvalho AS, Machado EC, Ribeiro RV (2022) Water stress signaling and hydraulic traits in three congeneric citrus species under water deficit. Plant Sci 319:111255

    Article  CAS  PubMed  Google Scholar 

  • Moro CF, Gaspar M, da Silva FR, Pattathil S, Hahn MG, Salgado I, Braga MR (2017) S-nitrosoglutathione promotes cell wall remodelling, alters the transcriptional profile and induces root hair formation in the hairless root hair defective 6 (rhd6) mutant of Arabidopsis thaliana. New Phytol 213:1771–1786

    Article  CAS  PubMed  Google Scholar 

  • Mourão Filho FDAA, Espinoza-Núñez E, Stuchi ES, Ortega EMM (2007) Plant growth, yield, and fruit quality of ‘Fallglo’ and ‘Sunburst’ mandarins on four rootstocks. Sci Hortic 114:45–49

    Article  Google Scholar 

  • Pagnussat G, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedroso FKJV, Prudente DA, Bueno ACR, Machado EC, Ribeiro RV (2014) Drought tolerance in citrus trees is enhanced by rootstock-dependent changes in root growth and carbohydrate availability. Environ Exp Bot 101:26–35

    Article  CAS  Google Scholar 

  • Pissolato MD, Silveira NM, Prataviera PJC, Machado EC, Seabra AB, Pelegrino MT, Sodek L, Ribeiro RV (2020) Enhanced nitric oxide synthesis through nitrate supply improves drought tolerance of sugarcane plants. Front Plant Sci 11:970

    Article  PubMed  PubMed Central  Google Scholar 

  • Pompeu-Jr P, Salva R, Blumer S (2004) Copas e porta-enxertos nos viveiros de mudas cítricas do estado de São Paulo. Laranja 25:413–422

    Google Scholar 

  • Ribeiro RV, Espinoza-Núñez E, Junior JP, Machado EC (2014) Citrus rootstocks for improving the horticultural performance and physiological responses under constraining environments. In: Ahmad P et al (eds) Improvement of crops in the era of climatic changes. Springer, New York, pp 1–37

    Google Scholar 

  • Silva SF, Miranda MT, Cunha CP, Domingues-Jr AP, Aricetti JA, Caldana C, Machado EC, Ribeiro RV (2022) Metabolic profiling of drought tolerance: revealing how citrus rootstocks modulate plant metabolism under varying water availability. Environ Exp Bot 206:105169

    Article  Google Scholar 

  • Silveira NM, Frungillo L, Marcos FCC, Pelegrino MT, Miranda MT, Seabra AB, Salgado I, Machado EC, Ribeiro RV (2016) Exogenous nitric oxide improves sugarcane growth and photosynthesis under water deficit. Planta 244:181–190

    Article  CAS  PubMed  Google Scholar 

  • Silveira NM, Hancock JT, Frungillo L, Siasou E, Marcos FCC, Salgado I, Machado EC, Ribeiro RV (2017a) Evidence towards the involvement of nitric oxide in drought tolerance of sugarcane. Plant Physiol Biochem 115:354–359

    Article  CAS  PubMed  Google Scholar 

  • Silveira NM, Marcos FCC, Frungillo L, Moura BB, Seabra AB, Salgado I, Machado EC, Hancock JT, Ribeiro RV (2017b) S-nitrosoglutathione spraying improves stomatal conductance, Rubisco activity and antioxidant defense in both leaves and roots of sugarcane plants under water deficit. Physiol Plant 160:383–395

    Article  CAS  PubMed  Google Scholar 

  • Silveira NM, Seabra AB, Machado EC, Hancock JT, Ribeiro RV (2019a) Nitric oxide induced tolerance in plants under environmental limiting conditions. In: Hasanuzzaman M, Nahar K, Fujita M, Oku H, Islam T (eds) Approaches for enhancing abiotic stress tolerance in plants. Taylor & Francis Group, Bangladesh, pp 369–383

    Google Scholar 

  • Silveira NM, Machado EC, Ribeiro RV (2019b) Extracellular and intracellular NO detection in plants by diaminofluoresceins. In: Hancock TJ, Conway M (eds) Redox mediated signal transduction: methods and protocols, methods in molecular biology. Centre for Research in Biosciences, New York, pp 103–108

    Chapter  Google Scholar 

  • Silveira NM, Ribeiro RV, De Morais SF, De Souza SC, Silva SF, Seabra AB, Hancock JT, Machado EC (2021) Leaf arginine spraying improves leaf gas exchange under water deficit and root antioxidant responses during the recovery period. Plant Physiol Biochem 162:315–326

    Article  CAS  PubMed  Google Scholar 

  • Tardieu F (1996) Drought perception by plants. Do cells of droughted plants experience water stress? Plant Growth Regul 20:93–104

    Article  CAS  Google Scholar 

  • Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci 6:534

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu XT, ** X, Liao WB, Dawuda MM, Li XP, Wang M, Niu LJ, Ren PJ, Zhu YC (2017) Nitric oxide is involved in ethylene-induced adventitious root development in cucumber (Cucumis sativus L.) explants. Sci Hortic 215:65–71

    Article  CAS  Google Scholar 

Download references

Acknowledgements

NMS acknowledges the fellowship granted by the National Council for Scientific and Technological Development (CNPq, Brazil, Grant No. 150050/2022-4). The authors acknowledge the São Paulo Research Foundation (FAPESP, Brazil; Grant No. 2019/15276-8) as well as the scholarship to MTM (Grant No. 2018/09834-5). RVR and ECM are fellows of the CNPq, and MIMO acknowledges the scholarship granted by PIBIC/CNPq/IAC. The authors are thankful to Prof. Dr. Maria Andréia Delbin (UNICAMP, Brazil) for hel** us with the fluorescence microscopy analyses.

Author information

Authors and Affiliations

  1. Laboratory of Crop Physiology, Department of Plant Biology, Institute of Biology, University of Campinas (UNICAMP), Campinas, SP, Brazil

    Neidiquele M. Silveira, Simone F. da Silva & Rafael V. Ribeiro

  2. Department of Biodiversity, Institute of Biosciences, São Paulo State University (UNESP), Rio Claro, SP, Brazil

    Neidiquele M. Silveira

  3. Laboratory of Plant Physiology “Coaracy M. Franco”, Center R&D of Agricultural Biosystems and Post-Harvest, Agronomic Institute (IAC), Campinas, SP, Brazil

    Maria Isabel M. de Oliveira, Marcela T. Miranda & Eduardo C. Machado

  4. Laboratory of Plant Anatomy, Department of Plant Biology, Institute of Biology, University of Campinas (UNICAMP), Campinas, SP, Brazil

    Matheus P. Passos

Authors
  1. Neidiquele M. Silveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Isabel M. de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simone F. da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcela T. Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matheus P. Passos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eduardo C. Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rafael V. Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NMS, ECM and RVR designed the experiments. NMS, MIMO, SFS and MTM took the measurements of plant biometry and collection of plant material. MPP assisted in the fluorescence microscopy analysis. NMS and RVR wrote the manuscript, and all authors contributed to data discussion and edited the final version of the manuscript.

Corresponding authors

Correspondence to Neidiquele M. Silveira or Rafael V. Ribeiro.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

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.

Supplementary file1 (DOCX 269 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silveira, N.M., de Oliveira, M.I.M., da Silva, S.F. et al. Enhanced root growth and nitric oxide content in ‘Mandarin’ lime under drought stress: experimental evidence. Braz. J. Bot 47, 13–18 (2024). https://doi.org/10.1007/s40415-023-00964-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-023-00964-y

Keywords

Search

Navigation