Seed priming with microalgae enhances plant productivity and rhizosphere health

Highlights

	● Priming of dwarf pea seeds with microalgal strains significantly enhanced plant growth
	● Rhizosphere health also improved upon priming of seeds with microalgal strains
	● Microalgae boost soil health, C/N content, EPS, IAA, and DHA in soils
	● Plant growth and rhizosphere health improvements due to priming are soil-specific

Abstract

Microalgae play a key role as primary colonizers of soil, enhancing plant growth and improving soil health. Seed priming is a widely used method to improve seedling performance, counteract soil-related stresses, and boost plant productivity. Here we investigated the impact of priming dwarf pea seeds with live cells or disrupted cell mass of two microalgae, Desmodesmus sp. MAS1 and Heterochlorella sp. MAS3, on plant growth response and rhizosphere health. Plant growth metrics, rhizosphere health parameters, and nutrient status indicators were investigated 21 days after sowing in two different soils (designated as A and B) with varying pH. Results revealed that priming significantly improved the biochemistry of rhizosphere in soil B (pH 8), with over 30% increases in leaf count and fresh weight compared to soil A (pH 6). While flowering rates remained low, priming with strain MAS1 significantly enhanced chlorophyll (20%), indole-3-acetic acid (61%), and dehydrogenase activity (50%). Furthermore, strain MAS1 boosted nutrient availability in the rhizosphere, with a 30%–60% increase in carbon and nitrogen levels, promoting exopolysaccharide release. Our findings thus demonstrate the potential of seed priming with microalgae in modulating rhizosphere health, thereby enhancing plant growth and productivity.

Graphical abstract

Keywords

rhizosphere / seed priming / soil health / microalgae / seaweed extract

References

[1] Abinandan, S., Shanthakumar, S., Panneerselvan, L., Venkateswarlu, K., Megharaj, M., 2022. Algalization of acid soils with Desmodesmus sp. MAS1 and Heterochlorella sp. MAS3 enriches bacteria of ecological importance. ACS Agricultural Science & Technology 2, 512–520.

[2] Arafa, S.A., Attia, K.A., Niedbała, G., Piekutowska, M., Alamery, S., Abdelaal, K., Alateeq, T.K., Ali, M.A.M., Elkelish, A., Attallah, S.Y., 2021. Seed priming boost adaptation in pea plants under drought stress. Plants10, 2201.

[3] Band, L.R., Úbeda-Tomás, S., Dyson, R.J., Middleton, A.M., Hodgman, T.C., Owen, M.R., Jensen, O.E., Bennett, M.J., King, J.R., 2012. Growth-induced hormone dilution can explain the dynamics of plant root cell elongation. Proceedings of the National Academy of Sciences of the United States of America109, 7577–7582.

[4] Bhattacharjee, A., Thompson, A.M., Schwarz, K.C., Burnet, M.C., Kim, Y.M., Nunez, J.R., Fansler, S.J., Farris, Y., Brislawn, C.J., Metz, T.O., McClure, R.S., Renslow, R.S., Shor, L., Jansson, J.K., Hofmockel, K.S., Anderton, C.R., 2020. Soil microbial EPS resiliency is influenced by carbon source accessibility. Soil Biology and Biochemistry151, 108037.

[5] Chai, Y.N., Futrell, S., Schachtman, D.P., 2022. Assessment of bacterial inoculant delivery methods for cereal crops. Frontiers in Microbiology13, 791110.

[6] Chua, M., Erickson, T.E., Merritt, D.J., Chilton, A.M., Ooi, M.K.J., Muñoz–Rojas, M., 2020. Bio–priming seeds with cyanobacteria: effects on native plant growth and soil properties. Restoration Ecology28, S168–S176.

[7] Dijkstra, F.A., Carrillo, Y., Pendall, E., Morgan, J.A., 2013. Rhizosphere priming: a nutrient perspective. Frontiers in Microbiology,4, 216.

[8] DuBois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry28, 350–356.

[9] Eldridge, D.J., Greene, R.S.B., 1994. Microbiotic soil crusts – a review of their roles in soil and ecological processes in the rangelands of Australia. Soil Research32, 389–415.

[10] Etesami, H., Jeong, B.R., Glick, B.R., 2023. Potential use of Bacillus spp. as an effective biostimulant against abiotic stresses in crops—A review. Current Research in Biotechnology5, 100128.

[11] Henneron, L., Kardol, P., Wardle, D.A., Cros, C., Fontaine, S., 2020. Rhizosphere control of soil nitrogen cycling: a key component of plant economic strategies. New Phytologist228, 1269–1282.

[12] Imran, M., Mahmood, A., Römheld, V., Neumann, G., 2013. Nutrient seed priming improves seedling development of maize exposed to low root zone temperatures during early growth. European Journal of Agronomy49, 141–148.

[13] Labeeuw, L., Khey, J., Bramucci, A.R., Atwal, H., de la Mata, A.P., Harynuk, J., Case, R.J., 2016. Indole–3–acetic acid is produced by Emiliania huxleyi coccolith–bearing cells and triggers a physiological response in bald cells. Frontiers in Microbiology7, 828.

[14] Lee, S.M., Ryu, C.M., 2021. Algae as new kids in the beneficial plant microbiome. Frontiers in Plant Science12, 599742.

[15] Li, Y., He, N.P., Hou, J.H., Xu, L., Liu, C.C., Zhang, J.H., Wang, Q.F., Zhang, X.M., Wu, X.Q., 2018. Factors influencing leaf chlorophyll content in natural forests at the biome scale. Frontiers in Ecology and Evolution6, 64.

[16] Liang, Y., Niu, Y., Gao, Y., Zhang, Y., Zhang, X., 2021. The role of extracellular polymeric substances in microalgae and their potential applications in environmental remediation. Journal of Environmental Management 287, 112341.

[17] Ludidi, N.N., Pellny, T.K., Kiddle, G., Dutilleul, C., Groten, K., Van Heerden, P.D.R., Dutt, S., Powers, S.J., Römer, P., Foyer, C.H., 2007. Genetic variation in pea (Pisum sativum L.) demonstrates the importance of root but not shoot C/N ratios in the control of plant morphology and reveals a unique relationship between shoot length and nodulation intensity. Plant, Cell & Environment 30, 1256–1268.

[18] Lukešová, A., 2001. Soil algae in brown coal and lignite post‐mining areas in central europe (Czech Republic and Germany). Restoration Ecology9, 341–350.

[19] Luo, L., Xu, L., Chen, Z., 2020. Mechanisms of microalgae–bacteria interactions for enhanced nutrient removal from wastewater. Bioresource Technology 303, 122948.

[20] Majda, C., Khalid, D., Aziz, A., Rachid, B., Badr, A.S., Lotfi, A., Mohamed, B., 2019. Nutri–priming as an efficient means to improve the agronomic performance of molybdenum in common bean (Phaseolus vulgaris L. ). Science of the Total Environment661, 654–663.

[21] Martínez–Viveros, O., Jorquera, M.A., Crowley, D.E., Gajardo, G., Mora, M.L., 2010. Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. Journal of Soil Science and Plant Nutrition10, 293–319.

[22] Mashabela, M.D., Tugizimana, F., Steenkamp, P.A., Piater, L.A., Dubery, I.A., Mhlongo, M., 2022. Untargeted metabolite profiling to elucidate rhizosphere and leaf metabolome changes of wheat cultivars (Triticum aestivum L.) treated with the plant growth–promoting rhizobacteria Paenibacillus alvei (T22) and Bacillus subtilis. Frontiers in Microbiology 13, 971836.

[23] Michalak, I., Miller, U., Tuhy, Ł., Sówka, I., Chojnacka, K., 2017. Characterisation of biological properties of co‐composted baltic seaweeds in germination tests. Engineering in Life Sciences17, 153–164.

[24] Mückschel, F., Ollo, E., Glaeser, S.P., Düring, R., Yan, F., Velten, H., Theilen, U., Frei, M., 2023. Nitrogen use efficiency of microalgae application in wheat compared to mineral fertilizer. Journal of Plant Nutrition and Soil Science186, 522–531.

[25] Muñoz–Rojas, M., Chilton, A., Liyanage, G.S., Erickson, T.E., Merritt, D.J., Neilan, B.A., Ooi, M.K.J., 2018. Effects of indigenous soil cyanobacteria on seed germination and seedling growth of arid species used in restoration. Plant and Soil429, 91–100.

[26] Mutale–Joan, C., Redouane, B., Najib, E., Yassine, K., Lyamlouli, K., Laila, S., Zeroual, Y., Hicham, E.A., 2020. Screening of microalgae liquid extracts for their bio stimulant properties on plant growth, nutrient uptake and metabolite profile of Solanum lycopersicum L. Scientific Reports10, 2820.

[27] Nath, A., Das, P., Gupta, P., 2021. Soil carbon sequestration in agriculture: opportunities and challenges. Journal of Soil Science and Plant Nutrition 21, 963–979.

[28] Oliveira, R.S., Rocha, I., Ma, Y., Vosátka, M., Freitas, H., 2016. Seed coating with arbuscular mycorrhizal fungi as an ecotechnologicalapproach for sustainable agricultural production of common wheat (Triticum aestivum L. ). Journal of Toxicology and Environmental Health, Part A79, 329–337.

[29] Paparella, S., Araújo, S.S., Rossi, G., Wijayasinghe, M., Carbonera, D., Balestrazzi, A., 2015. Seed priming: state of the art and new perspectives. Plant Cell Reports34, 1281–1293.

[30] Praveen, K., Abinandan, S., Venkateswarlu, K., Megharaj, M., 2024a. Leveraging Phenotypic traits in microalgae: a novel strategy for wastewater treatment and sustainable biomass production. ACS ES&T Water4, 103–113.

[31] Praveen, K., Abinandan, S., Venkateswarlu, K., Megharaj, M., 2024b. Harnessing extremophilic trait and metabolic flexibility of microalgal strains for the treatment of highly alkaline winery wastewater. ACS ES&T Engineering4, 455–465.

[32] Ramakrishnan, B., Maddela, N.R., Venkateswarlu, K., Megharaj, M., 2023. Potential of microalgae and cyanobacteria to improve soil health and agricultural productivity: a critical view. Environmental Science Advances2, 586–611.

[33] Ronga, D., Biazzi, E., Parati, K., Carminati, D., Carminati, E., Tava, A., 2019. Microalgal biostimulants and biofertilisers in crop productions. Agronomy,9, 192.

[34] Rupawalla, Z., Shaw, L., Ross, I.L., Schmidt, S., Hankamer, B., Wolf, J., 2022. Germination screen for microalgae–generated plant growth biostimulants. Algal Research66, 102784.

[35] Salem, D.M.S.A., El Sikaily, A., Abou–Taleb, E.A., 2018. Nutritional value and health quotient of algae collected from egyptian coast, Alexandria. Egyptian Journal of Aquatic Biology & Fisheries22, 419–429.

[36] Shanthakumar, S., Abinandan, S., Venkateswarlu, K., Subashchandrabose, S.R., Megharaj, M., 2021. Algalization of acid soils with acid‐tolerant strains: improvement in pH, carbon content, exopolysaccharides, indole acetic acid and dehydrogenase activity. Land Degradation & Development32, 3157–3166.

[37] Sivaram, A.K., Logeshwaran, P., Subashchandrabose, S.R., Lockington, R., Naidu, R., Megharaj, M., 2018. Comparison of plants with C₃ and C₄ carbon fixation pathways for remediation of polycyclic aromatic hydrocarbon contaminated soils. Scientific Reports8, 2100.

[38] Supraja, K.V., Behera, B., Balasubramanian, P., 2020. Efficacy of microalgal extracts as biostimulants through seed treatment and foliar spray for tomato cultivation. Industrial Crops and Products151, 112453.

[39] Torres–Cortés, G., Bonneau, S., Bouchez, O., Genthon, C., Briand, M., Jacques, M.A., Barret, M., 2018. Functional microbial features driving community assembly during seed germination and emergence. Frontiers in Plant Science9, 902.

[40] Tsai, S.S., Chang, Y.C.A., 2022. Plant maturity affects flowering ability and flower quality in Phalaenopsis, focusing on their relationship to carbon–to–nitrogen ratio. HortScience57, 191–196.

[41] Ullah, A., Farooq, M., Qadeer, A., Sanaullah, M., 2022. Impact of zinc and plant growth‐promoting bacteria on soil health as well as aboveground biomass of desi and kabuli chickpea under arid conditions. Journal of the Science of Food and Agriculture102, 2262–2269.

[42] ur Rehman, H., Iqbal, H., Basra, S.M.A., Afzal, I., Farooq, M., Wakeel, A., Wang, N., 2015. Seed priming improves early seedling vigor, growth and productivity of spring maize. Journal of Integrative Agriculture14, 1745–1754.

[43] Vain, S., Tamm, I., Tamm, Ü., Annusver, M., Zobel, K., 2023. Negative relationship between topsoil root production and grain yield in oat and barley. Agriculture, Ecosystems & Environment349, 108467.

[44] Wakelin, S.A., Matson, A., Wigley, K., Waller, L., Dickie, I.A., Whitehead, D., Garrett, L., 2021. High maintenance of rhizosphere soil C and N equilibrium regardless of plant species or species traits. Frontiers in Soil Science1, 762510.

[45] Wasilewska, L.D., Bralczyk, J., Szczegielniak, J., 1987. The role of gibberellin in regulation of dwarf plants development. Plant Science53, 11–19.

[46] Wei, X.L., Fu, T.L., He, G.D., Zhong, Z.Y., Yang, M.F., Lou, F., He, T.B., 2023. Characteristics of rhizosphere and bulk soil microbial community of Chinese cabbage (Brassica campestris) grown in Karst area. Frontiers in Microbiology14, 1241436.

[47] Wingender, J., Neu, T.R., Flemming, H.C., 1999. What are bacterial extracellular polymeric substances? In: Wingender, J., Neu, T.R., Flemming, H.C., eds. Microbial Extracellular Polymeric Substances. Berlin Heidelberg: Springer, 1–19.

[48] Yasmeen, A., Nouman, W., Basra, S.M.A., Wahid, A., ur-Rehman, H., Hussain, N., Afzal, I., 2014. Morphological and physiological response of tomato (Solanum lycopersicum L. ) to natural and synthetic cytokinin sources: a comparative study. Acta Physiologiae Plantarum36, 3147–3155.

[49] Zhang, X., Koehler, H., 2022. Soil algae for combating soil degradation – greenhouse experiment with different soil amendments. Soil Research61, 70–82.

[50] Zhang, Y.F., Chen, C., Jin, Z.X., Yang, Z.N., Li, Y.L., 2022. Leaf anatomy, photosynthesis, and chloroplast ultrastructure of Heptacodium miconioides seedlings reveal adaptation to light environment. Environmental and Experimental Botany195, 104780.

CRediT authorship contribution statement

Abinandan Sudharsanam, Praveen Kuppan: Investigation, Methodology, Writing–original draft; Venkateswarlu Kadiyala: Writing–review & editing; Mallavarapu Megharaj: Conceptualization, Formal analysis, Funding acquisition, Methodology, Resources, Supervision, Writing–review & editing.

Declaration of competing interest

The authors declare no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

PK acknowledges the VC Scholarship provided by the University of Newcastle (UoN) and Wine Australia. This work was supported by Wine Australia with levies from Australia’s grape growers and winemakers and matching funds from the Australian Government.

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2024 Higher Education Press