Leaf manganese and phenolics as proxies of soil acidification and phosphorus acquisition mechanisms in lentil cultivars on alkaline soil
Georgia S. Theologidou A , Ioannis Ipsilantis B and Ioannis T. Tsialtas
A *
A
B
Abstract
Leaf manganese (Mn) concentration has been used as a proxy for root exudation and phosphorus (P) uptake under controlled conditions, but there are limited field studies that confirm its validity. On an alkaline, P-poor soil, four lentil cultivars (‘Samos’, ‘Thessaly’, ‘Flip’, ‘Algeria’) received two P rates (0 and 26.2 kg P ha−1), for two growing seasons, to study whether aboveground assessments [leaf P, Mn, phenolic concentration (TPhe)] can approximate rhizosphere physiological traits related to P acquisition [soil acidification (ΔpH), arbuscular mycorrhizal fungi (AMF) colonisation, acid phosphatase activity (APase)]. Phosphorus addition had no effect on the determined traits. Cultivars differed in leaf P, Mn, TPhe and AMF, but there was no clear pattern relating aboveground traits to rhizosphere traits related to P acquisition, thus not confirming that leaf Mn can be a proxy of root exudation. Of three growth stages [V 7–8, R1 (first bloom), R4 (flat pod)], R1 seemed to be critical, showing the highest leaf P, ΔpH, AMF and TPhe. Precipitation and temperatures over the growing season were determinants of lentil responses affecting rhizosphere activity, soil P availability and finally leaf traits. In conclusion, in lentil on alkaline and P-limiting soils, high leaf Mn and phenolic concentration are not reliable indicators of rhizosphere P-acquiring mechanisms.
Keywords: acid phosphatase activity, alkalinity, carboxylates, exudation, grain legumes, Mediterranean soils, mycorrhiza, soil pH.
References
Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biology 3, 139-148.
| Crossref | Google Scholar |
Baird JM, Walley FL, Shirtliffe SJ (2010) Arbuscular mycorrhizal fungi colonization and phosphorus nutrition in organic field pea and lentil. Mycorrhiza 20, 541-549.
| Crossref | Google Scholar | PubMed |
Barrow NJ (2017) The effects of pH on phosphate uptake from the soil. Plant and Soil 410, 401-410.
| Crossref | Google Scholar |
Barrow NJ, Debnath A, Sen A (2021) Effect of pH and prior treatment with phosphate on the rate and amount of reaction of soils with phosphate. European Journal of Soil Science 72, 243-253.
| Crossref | Google Scholar |
Brennan RF, Bolland MDA (2003) Application of fertilizer manganese doubled yields of lentil grown on alkaline soils. Journal of Plant Nutrition 26, 1263-1276.
| Crossref | Google Scholar |
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 245, 35-47.
| Crossref | Google Scholar |
de-Bashan LE, Magallon-Servin P, Lopez BR, Nannipieri P (2022) Biological activities affect the dynamic of P in dryland soils. Biology and Fertility of Soils 58, 105-119.
| Crossref | Google Scholar |
Del-Saz NF, Romero-Munar A, Cawthray GR, Aroca R, Baraza E, Flexas J, Lambers H, Ribas-Carbó M (2017) Arbuscular mycorrhizal fungus colonization in Nicotiana tabacum decreases the rate of both carboxylate exudation and root respiration and increases plant growth under phosphorus limitation. Plant and Soil 416, 97-106.
| Crossref | Google Scholar |
Erskine W, Muehlbauer FJ, Short RW (1990) Stages of development in lentil. Experimental Agriculture 26, 297-302.
| Crossref | Google Scholar |
Ganguly S, Roy A, Murmu SK, Sagolsem D, Sarkar M, Sen S, Das D, Das C, Chakraborty P, Bhattacharyya PK, Nath R, Tripathi K, Sarker A, Bhattacharyya S (2021) Variation in P-acquisition ability and acid phosphatase activity at the early vegetative stage of lentil and their validation on P-deficiency field. Acta Physiologiae Plantarum 43, 109.
| Crossref | Google Scholar |
George TS, French AS, Brown LK, Karley AJ, White PJ, Ramsay L, Daniell TJ (2014) Genotypic variation in the ability of landraces and commercial cereal varieties to avoid manganese deficiency in soils with limited manganese availability: is there a role for root-exuded phytases? Physiologia Plantarum 151, 243-256.
| Crossref | Google Scholar | PubMed |
Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Annals of Botany 94, 323-332.
| Crossref | Google Scholar | PubMed |
Honvault N, Houben D, Nobile C, Firmin S, Lambers H, Faucon M-P (2021) Tradeoffs among phosphorus-acquisition root traits of crop species for agroecological intensification. Plant and Soil 461, 137-150.
| Crossref | Google Scholar |
Huang G, Hayes PE, Ryan MH, Pang J, Lambers H (2017) Peppermint trees shift their phosphorus-acquisition strategy along a strong gradient of plant-available phosphorus by increasing their transpiration at very low phosphorus availability. Oecologia 185, 387-400.
| Crossref | Google Scholar | PubMed |
Ipsilantis I, Theologidou GS, Bilias F, Karypidou A, Kalyvas A, Tsialtas IT (2022) Phosphorus fertilisation may induce Zn deficiency in cotton (Gossypium hirsutum) on calcareous Mediterranean soils. Functional Plant Biology 49, 382-391.
| Crossref | Google Scholar | PubMed |
Juszczuk IM, Wiktorowska A, Malusá E, Rychter AM (2004) Changes in the concentration of phenolic compounds and exudation induced by phosphate deficiency in bean plants (Phaseolus vulgaris L.). Plant and Soil 267, 41-49.
| Crossref | Google Scholar |
Khademi Z, Jones DL, Malakouti MJ, Asadi F, Ardebili M (2009) Organic acid mediated nutrient extraction efficiency in three calcareous soils. Australian Journal of Soil Research 47, 213-220.
| Crossref | Google Scholar |
Kuo S (1996) Phosphorus. In ‘Methods of soil analysis, Part 3, Chemical methods’. (Eds DL Sparks, AL Page, PA Helmke, et al.) pp. 869–919. (Soil Science Society of America: Madison, WI, USA) doi:10.2136/sssabookser5.3.c32
Lahiri K, Chattopadhyay S, Chatterjee S, Ghosh B (1993) Biochemical changes in nodules of Vigna mungo (L.) during vegetative and reproductive stages of plant growth in the field. Annals of Botany 71, 485-488.
| Crossref | Google Scholar |
Lambers H, Hayes PE, Laliberté E, Oliveira RS, Turner BL (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends in Plant Science 20, 83-90.
| Crossref | Google Scholar | PubMed |
Lambers H, Wright IJ, Guilherme Pereira C, Bellingham PJ, Bentley LP, Boonman A, Cernusak LA, Foulds W, Gleason SM, Gray EF, Hayes PE, Kooyman RM, Malhi Y, Richardson SJ, Shane MW, Staudinger C, Stock WD, Swarts ND, Turner BL, Turner J, Veneklaas EJ, Wasaki J, Westoby M, Xu Y (2021) Leaf manganese concentrations as a tool to assess belowground plant functioning in phosphorus-impoverished environments. Plant and Soil 461, 43-61.
| Crossref | Google Scholar |
Maathuis FJM (2009) Physiological functions of mineral macronutrients. Current Opinion in Plant Biology 12, 250-258.
| Crossref | Google Scholar | PubMed |
Maltais-Landry G (2015) Legumes have a greater effect on rhizosphere properties (pH, organic acids and enzyme activity) but a smaller impact on soil P compared to other cover crops. Plant and Soil 394, 139-154.
| Crossref | Google Scholar |
Maltais-Landry G, Scow K, Brennan E (2014) Soil phosphorus mobilization in the rhizosphere of cover crops has little effect on phosphorus cycling in California agricultural soils. Soil Biology and Biochemistry 78, 255-262.
| Crossref | Google Scholar |
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115, 495-501.
| Crossref | Google Scholar | PubMed |
Menezes-Blackburn D, Giles C, Darch T, George TS, Blackwell M, Stutter M, Shand C, Lumsdon D, Cooper P, Wendler R, Brown L, Almeida DS, Wearing C, Zhang H, Haygarth PM (2018) Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: a review. Plant and Soil 427, 5-16.
| Crossref | Google Scholar | PubMed |
Nazeri NK, Lambers H, Tibbett M, Ryan MH (2014) Moderating mycorrhizas: arbuscular mycorrhizas modify rhizosphere chemistry and maintain plant phosphorus status within narrow boundaries. Plant, Cell and Environment 37, 911-921.
| Crossref | Google Scholar | PubMed |
Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KHM (2018) The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytologist 219, 518-529.
| Crossref | Google Scholar | PubMed |
Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant and Soil 288, 127-139.
| Crossref | Google Scholar |
Phillips DA, Tsai SM (1992) Flavonoids as plant signals to rhizosphere microbes. Mycorrhiza 1, 55-58.
| Crossref | Google Scholar |
Rengel Z (2002) Genetic control of root exudation. Plant and Soil 245, 59-70.
| Crossref | Google Scholar |
Rengel Z (2015) Availability of Mn, Zn and Fe in the rhizosphere. Journal of Soil Science and Plant Nutrition 15, 397-409.
| Crossref | Google Scholar |
Reynolds M, Chapman S, Crespo-Herrera L, Molero G, Mondal S, Pequeno DNL, Pinto F, Pinera-Chavez FJ, Poland J, Rivera-Amado C, Saint Pierre C, Sukumaran S (2020) Breeder friendly phenotyping. Plant Science 295, 110396.
| Crossref | Google Scholar | PubMed |
Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagents. Methods in Enzymology 299, 152-178.
| Crossref | Google Scholar |
Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint J-P, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12, 1290-1306.
| Crossref | Google Scholar | PubMed |
Sylvia DM (1994) Vesicular-arbuscular mycorrhizal (VAM) fungi. In ‘Methods of soil analysis, Part 2, Microbiological and biochemical properties’. Soil Science Society of America Book Series, No. 5. (Eds RW Weaver, JS Angle, PS Bottomley) pp. 351–378. (Soil Science Society of America: Madison, WI, USA)
Theologidou GS, Ipsilantis I, Tsialtas IT (2023) Phosphorus effects on four lentil cultivars grown on alkaline Mediterranean soil. Nutrient Cycling in Agroecosystems 125, 1-14.
| Crossref | Google Scholar |
Wang Y, Lambers H (2020) Root-released organic anions in response to low phosphorus availability: recent progress, challenges and future perspectives. Plant and Soil 447, 135-156.
| Crossref | Google Scholar |
Wang Y, Krogstad T, Clarke JL, Hallama M, Øgaard AF, Eich-Greatorex S, Kandeler E, Clarke N (2016) Rhizosphere organic anions play a minor role in improving crop species’ ability to take up residual phosphorus (P) in agricultural soils low in P availability. Frontiers in Plant Science 7, 1664.
| Crossref | Google Scholar | PubMed |
Wang Y, Krogstad T, Clarke N, Øgaard AF, Clarke JL (2017) Impact of phosphorus on rhizosphere organic anions of wheat at different growth stages under field conditions. AoB PLANTS 9, plx008.
| Crossref | Google Scholar |
Wen Z, Li H, Shen Q, Tang X, Xiong C, Li H, Pang J, Ryan MH, Lambers H, Shen J (2019) Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytologist 223, 882-895.
| Crossref | Google Scholar | PubMed |
Ylivainio K, Peltovuori T (2012) Phosphorus acquisition by barley (Hordeum vulgare L.) at suboptimal soil temperature. Agricultural and Food Science 21, 453-461.
| Crossref | Google Scholar |
