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Plant function and evolutionary biology
RESEARCH ARTICLE

Barley plants carrying the altered function Sln1d allele display modified responses to low phosphorus supply: implications for phosphorus utilisation efficiency

Leonardo Gualano A , Jorge I. Moriconi A , Sonia Oliferuk A , Martha Silva A , Gabriela E. Tranquilli B and Guillermo E. Santa-María https://orcid.org/0000-0002-3998-8517 A C
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A Instituto Tecnológico Chascomús (INTECH), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de San Martín (CONICET-UNSAM), Avenida Intendente Marino, km 8.2, Chascomús, 7130, Buenos Aires, Argentina.

B Instituto Nacional de Tecnología Agropecuaria (INTA), Centro de Investigación de Recursos Naturales, Instituto de Recursos Biológicos. Castelar. N. Repetto y Los Reseros s/n. Hurlingham, 1686, Provincia de Buenos Aires, Argentina.

C Corresponding author. Email: gsantama@intech.gov.ar

Functional Plant Biology 48(8) 780-792 https://doi.org/10.1071/FP19250
Submitted: 26 August 2019  Accepted: 15 February 2021   Published: 15 March 2021

Abstract

The module GA-GID1-DELLA (Gibberellin-Gibberellin Receptor-DELLA proteins) provides a point for the integration of signals potentially relevant in determining nutrient utilisation and acquisition efficiencies. In this study, we explored the role of components of this module during the acclimation of barley plants (Hordeum vulgare L.) to different phosphorus (P) supplies by using two related genotypes, harbouring either the WT or the Sln1d alleles of the DELLA-coding gene Sln1. Dwarf Sln1d plants exhibited reduced shoot P utilisation efficiency (PUtE) and better performance at low levels of P supply. The superior PUtE displayed by WT plants disappeared when corrected by internal P concentration, indicating that multiple analyses are necessary to fully understand the meaning of PUtE estimates. Over a wide range of external supplies of P, Sln1d plants displayed enhanced P concentration, which was associated with low relative growth rate, high biomass partitioning to roots and high P-uptake-rate, thus suggesting that the effect of the Sln1d allele on P dynamics is not simply a consequence of slow growth habit. An enhanced P concentration was also found in a mutant with defective GAs-synthesis. Our results suggest that components of the GA-GID1-DELLAs module contribute to set the acclimation response of barley plants to low P supply through both P-dynamics dependent and P-dynamics independent mechanisms.

Keywords: Hordeum vulgare L., nutrient use efficiency, phosphorus nutrition, phosphorus supply, barley.


References

Blanco-Touriñán N, Serrano-Mislata A, Alabadí D (2020) Regulation of DELLA proteins by post-translational modification. Plant & Cell Physiology 61, 1891–1901.
Regulation of DELLA proteins by post-translational modification.Crossref | GoogleScholarGoogle Scholar |

Chandler PM, Harding CA (2013) ‘Overgrowth’ mutants in barley and wheat: new alleles and phenotypes of the ‘Green Revolution’ DELLA gene. Journal of Experimental Botany 64, 1603–1613.
‘Overgrowth’ mutants in barley and wheat: new alleles and phenotypes of the ‘Green Revolution’ DELLA gene.Crossref | GoogleScholarGoogle Scholar | 23382550PubMed |

Chen Y, Rengel Z, Palta J, Siddique KHM (2018) Efficient root systems for enhancing tolerance of crops to water and phosphorus limitation. Indian Journal of Plant Physiology / Official Publication of the Indian Society for Plant Physiology 23, 689–696.
Efficient root systems for enhancing tolerance of crops to water and phosphorus limitation.Crossref | GoogleScholarGoogle Scholar |

Chien PS, Chiang CP, Leong SJ, Chiou TJ (2018) Sensing and signaling of phosphate starvation – from local to long distance. Plant & Cell Physiology 59, 1714–1722.
Sensing and signaling of phosphate starvation – from local to long distance.Crossref | GoogleScholarGoogle Scholar |

Cogliatti DH, Santa-María GE (1990) Influx and efflux of phosphorus in roots of wheat plants in non-growth-limiting concentrations of phosphorus. Journal of Experimental Botany 41, 601–607.
Influx and efflux of phosphorus in roots of wheat plants in non-growth-limiting concentrations of phosphorus.Crossref | GoogleScholarGoogle Scholar |

Ferrol N, Azcón-Aguilar C, Pérez-Tienda J (2019) Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved. Plant Science 280, 441–447.
Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved.Crossref | GoogleScholarGoogle Scholar | 30824024PubMed |

Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America 110, E5025–E5034.
DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 24297892PubMed |

Gallego-Bartolomé J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabadí D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Molecular Biology and Evolution 27, 1247–1256.
Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 20093430PubMed |

Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV (2002) Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiology 129, 191–200.
Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression.Crossref | GoogleScholarGoogle Scholar | 12011350PubMed |

Henry A, Chopra S, Clark DG, Lynch JP (2012) Responses to low phosphorus in high and low foliar anthocyanin coleus (Solenostemon scutellarioides) and maize (Zea mays). Functional Plant Biology 39, 255–265.
Responses to low phosphorus in high and low foliar anthocyanin coleus (Solenostemon scutellarioides) and maize (Zea mays).Crossref | GoogleScholarGoogle Scholar | 32480779PubMed |

Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiology 145, 1460–1470.
Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17932308PubMed |

Manske GGB, Ortiz-Monasterio JI, van Ginkel RM, Rajaram S, Vlek PLG (2002) Phosphorus use efficiency in tall, semi-dwarf and dwarf near-isogenic lines of spring wheat. Euphytica 125, 113–119.
Phosphorus use efficiency in tall, semi-dwarf and dwarf near-isogenic lines of spring wheat.Crossref | GoogleScholarGoogle Scholar |

Moriconi JI, Kotula L, Santa-María GE, Colmer TD (2019) Root phenotypes of dwarf and “overgrowth” SLN1 barley mutants, and implications for hypoxic stress tolerance. Journal of Plant Physiology 234–235, 60–70.
Root phenotypes of dwarf and “overgrowth” SLN1 barley mutants, and implications for hypoxic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 30665049PubMed |

Nadira UA, Ahmed IM, Wu F, Zhang G (2016) The regulation of root growth in response to phosphorus deficiency mediated by phytohormones in a Tibetan wild barley accession. Acta Physiologiae Plantarum 38, 105
The regulation of root growth in response to phosphorus deficiency mediated by phytohormones in a Tibetan wild barley accession.Crossref | GoogleScholarGoogle Scholar |

Oliferuk S, Ródenas R, Pérez A, Martínez V, Rubio F, Santa-María GE (2017) DELLAs contribute to set the growth and mineral composition of Arabidopsis thaliana plants grown under conditions of potassium deprivation. Journal of Plant Growth Regulation 36, 487–501.
DELLAs contribute to set the growth and mineral composition of Arabidopsis thaliana plants grown under conditions of potassium deprivation.Crossref | GoogleScholarGoogle Scholar |

Ozturk L, Eker S, Torun B, Cakmak I (2005) Variation in phosphorus efficiency among 73 bread and durum wheat genotypes grown in a phosphorus-deficient calcareous soil. Plant and Soil 269, 69–80.
Variation in phosphorus efficiency among 73 bread and durum wheat genotypes grown in a phosphorus-deficient calcareous soil.Crossref | GoogleScholarGoogle Scholar |

Pang J, Ryan MH, Lambers H, Siddique KHM (2018) Phosphorus acquisition and utilisation in crop legumes under global change. Current Opinion in Plant Biology 45, 248–254.
Phosphorus acquisition and utilisation in crop legumes under global change.Crossref | GoogleScholarGoogle Scholar | 29853281PubMed |

Pinthus MJ, Gale MD (1990) The effects of “gibberellin-insensitive” dwarfing alleles in wheat on grain weight and protein content. Theoretical and Applied Genetics 79, 108–112.
The effects of “gibberellin-insensitive” dwarfing alleles in wheat on grain weight and protein content.Crossref | GoogleScholarGoogle Scholar | 24226128PubMed |

Prerostova S, Kramna B, Dobrev PI, Gaudinova A, Marsik P, Fiala R, Knirsch V, Vanek T, Kuresova G, Vankova R (2018) Organ–specific hormonal cross-talk in phosphate deficiency. Environmental and Experimental Botany 153, 198–208.
Organ–specific hormonal cross-talk in phosphate deficiency.Crossref | GoogleScholarGoogle Scholar |

Rose TJ, Wissuwa M (2012) Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops. Advances in Agronomy 116, 185–217.
Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops.Crossref | GoogleScholarGoogle Scholar |

Rose TJ, Mori A, Julia CC, Wissuwa M (2016) Screening for internal phosphorus utilization efficiency: comparison of genotypes at equal shoot P content is critical. Plant and Soil 401, 79–91.
Screening for internal phosphorus utilization efficiency: comparison of genotypes at equal shoot P content is critical.Crossref | GoogleScholarGoogle Scholar |

Ryan PR, Liao M, Delhaize E, Rebetzke GJ, Weligama C, Spielmeyer W, James RA (2015) Early vigour improves phosphate uptake in wheat. Journal of Experimental Botany 66, 7089–7100.
Early vigour improves phosphate uptake in wheat.Crossref | GoogleScholarGoogle Scholar | 26320241PubMed |

Santa-María GE, Moriconi JI, Oliferuk S (2015) Internal efficiency of nutrient utilization: what is it and how to measure it during vegetative plant growth? Journal of Experimental Botany 66, 3011–3018.
Internal efficiency of nutrient utilization: what is it and how to measure it during vegetative plant growth?Crossref | GoogleScholarGoogle Scholar | 25922492PubMed |

Van De Velde K, Ruelens P, Geuten K, Rohde A, Van Der Straeten D (2017) Exploiting DELLA signaling in cereals. Trends in Plant Science 22, 880–893.
Exploiting DELLA signaling in cereals.Crossref | GoogleScholarGoogle Scholar | 28843766PubMed |

Velu G, Singh RP, Huerta J, Guzmán C (2017) Genetic impact of Rht dwarfing genes on grain micronutrients concentration in wheat. Field Crops Research 214, 373–377.
Genetic impact of Rht dwarfing genes on grain micronutrients concentration in wheat.Crossref | GoogleScholarGoogle Scholar | 29200604PubMed |

Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195, 306–320.
Opportunities for improving phosphorus-use efficiency in crop plants.Crossref | GoogleScholarGoogle Scholar |

Wolbang CM, Chandler PM, Smith JJ, Ross JJ (2004) Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiology 134, 769–776.
Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems.Crossref | GoogleScholarGoogle Scholar | 14730077PubMed |

Zhang Y, Zhou Y, Chen S, Liu J, Fan K, Li Z, Liu Z, Wenxiong L (2019) Gibberellins play dual roles in response to phosphate starvation of tomato seedlings, negatively in shoots but positively in roots. Journal of Plant Physiology 234–235, 145–153.
Gibberellins play dual roles in response to phosphate starvation of tomato seedlings, negatively in shoots but positively in roots.Crossref | GoogleScholarGoogle Scholar | 30807885PubMed |