Algae as New Kids in the Beneficial Plant Microbiome

Abstract

Previously, algae were recognized as small prokaryotic and eukaryotic organisms found only in aquatic habitats. However, according to a recent paradigm shift, algae are considered ubiquitous organisms, occurring in plant tissues as well as in soil. Accumulating evidence suggests that algae represent a member of the plant microbiome. New results indicate that plants respond to algae and activate related downstream signaling pathways. Application of algae has beneficial effects on plant health, such as plant growth promotion and disease control. Although accumulating evidence suggests that secreted compounds and cell wall components of algae induce physiological and structural changes in plants that protect against biotic and abiotic stresses, knowledge of the underlying mechanisms and algal determinants is limited. In this review, we discuss recent studies on this topic, and highlight the bioprotectant and biostimulant roles of algae as a new member of the plant beneficial microbiome for crop improvement.

Keywords: Chlorella; biological control; cyanobacteria; microalgae; microbiome; plant growth promotion (PGP); plant immunity.

FIGURE 1

Leaf and root colonization by cyanobacteria. (1) Cyanobacteria enter the leaf tissue through the stomata and colonize the intercellular space, forming a cyanobacterial loop. (2) On the root surface, cyanobacteria exhibit two types of colonization pattern; in the root hair, filaments of Anabaena and Nostoc species form loose colonies, and in the restricted zone on the root surface, specific Nostoc species form cyanobacterial colonies. (3) Co-inoculation with 2,4-dichlorophenoxy acetic acid (2,4-D) (synthetic auxin) and Nostoc spp. increases para-nodule formation and nitrogen fixation. A large number of Nostoc spp. isolates colonize the root endosphere and form para-nodules to fix nitrogen.

FIGURE 2

Beneficial effects of algae on plants. In plants, prokaryotic microalgae such as Nostoc and Anabaena, and eukaryotic microalgae such as Chlorella, act as biological control agents (1), abiotic stress tolerance enhancers (2), biofertilizers that promote plant growth and crop yield (3), and anti-aging agents that delay senescence and enhance plant robustness (4).

FIGURE 3

Algal determinants that act as plant protectants and stimulants. (A) Inhibitory compounds. Cyanobacteria reduce the population of pathogenic bacteria, fungi, and insect pests by producing antibiotic and pesticidal compounds. Cyanobacteria-derived 4,4′-dihydroxybiphenyl, norharmane, and diterpenoids exhibit antibacterial activity, and microalgal siderophores inhibit bacterial growth through iron (Fe) competition. In addition, cyanobacterial cell wall-degrading enzymes such as chitosanase, β-1,4-glucanase, and β-1,3-glucanase reduce fungal infection. Cyanotoxins such as anatoxin, microcystin, and nodularin can protect the host plant against insect pests. (B) Phytohormones. Microalgae-derived phytohormone-mimicking compounds modulate plant growth, immunity, and abiotic stress tolerance. Plant growth regulators such as auxin and cytokinin increase plant growth and development as well as crop yield. Algae species also produce jasmonic acid (JA), salicylic acid (SA), and ethylene (ET), which act as major defense-related hormones in land plants. In addition, microalgae also produce abscisic acid (ABA), a central regulator of abiotic stress tolerance. (C) Nutrition. Nitrogen-fixing cyanobacteria promote plant growth by supplying macronutrients such as nitrogen, phosphorus, and potassium. Additionally, microalgae-derived vitamins, including vitamins B1, B2, B3, and B12, elicit plant immune response against phytopathogens. (D) Polysaccharides. Polysaccharides extracted from cyanobacteria and eukaryotic microalgae increase immunity and abiotic stress tolerance of the host plant. (E) D-lactic acid. Exogenous application of D-lactic acid produced by Chlorella elicits plant immunity via activation of D-lactate metabolism and production of mitochondrial reactive oxygen species (ROS). Algal D-lactic acid might also enhance abiotic stress tolerance in host plant by regulating ROS production.