Apocarotenoids: Old and New Mediators of the Arbuscular Mycorrhizal Symbiosis

Abstract

Plants utilize hormones and other small molecules to trigger and coordinate their growth and developmental processes, adapt and respond to environmental cues, and communicate with surrounding organisms. Some of these molecules originate from carotenoids that act as universal precursors of bioactive metabolites arising through oxidation of the carotenoid backbone. This metabolic conversion produces a large set of compounds known as apocarotenoids, which includes the plant hormones abscisic acid (ABA) and strigolactones (SLs) and different signaling molecules. An increasing body of evidence suggests a crucial role of previously identified and recently discovered carotenoid-derived metabolites in the communication with arbuscular mycorrhizal (AM) fungi and the establishment of the corresponding symbiosis, which is one of the most relevant plant-fungus mutualistic interactions in nature. In this review, we provide an update on the function of apocarotenoid hormones and regulatory metabolites in AM symbiosis, highlighting their effect on both partners.

Keywords: abscisic acid; apocarotenoids; arbuscular mycorrhizal symbiosis; blumenols; carotenoids; mycorradicin; strigolactones; zaxinone.

Figure 1

Formation of apocarotenoids involved in mycorrhization. Nine-cis-epoxycarotenoid dioxygenase (NCED) enzymes catalyze the cleavage of 9-cis-violaxanthin—formed from all-trans-zeaxanthin through epoxidation and isomerization reactions—and 9’-cis-neoxanthin (not shown) into the ABA precursor xanthoxin and apo-12’-violaxanthinal (or apo-12-neoxanthinal, not shown) (Nambara and Marion-Poll, 2005). Xanthoxin is then further converted to ABA by SDR and AAO. Carotenoid cleavage dioxygenase (CCD) enzymes catalyze a set of different carotenoid and apocarotenoid cleavage reactions. The C₂₇ apocarotenoids β-apo-10’-carotenal and/or β-apo-10’-zeaxanthinal may be formed by CCD4 enzymes that cleave all-trans-bicyclic carotenoids (Bruno et al., 2015; Bruno et al., 2016). CCD7 has been also implicated in the formation of all-trans-β-apo-10’-carotenoids, which include the zaxinone precursor all-trans-β-apo-10’-zeaxanthinal (see below); however, in this case, a cis to trans isomerization must be postulated, as the apo-10’-carotenoids produced by CCD7 enzymes are 9-cis-configured (Alder et al., 2012; Bruno et al., 2014). Several enzymatic studies show that CCD1 enzymes can produce C₁₄ directly from carotenoids or—in a secondary cleavage reaction—from all-trans-β-apo-10’-carotenoids. In the case of mycorrhizal tissues, it is assumed that they use β-apo-10’-carotenoids as substrate to form precursors of mycorradicin and blumenols (structure shown as blumenol C), which accumulate in AM-colonized root and act as symbiosis signal in plant leaves, respectively (Floss et al., 2008b; Walter et al., 2010; Hou et al., 2016; Wang et al., 2018). Following β-carotene isomerization catalyzed by D27, the SL biosynthetic enzyme, CCD7, cleaves 9-cis-β-carotene into 9-cis-β-apo-10’-carotenal and β-ionone. This step is followed by the CCD8-catalyzed conversion of 9-cis-β-apo-10’-carotenal into carlactone. Carlactone, a central intermediate in SL biosynthesis, is further modified by cytochrome P450 enzymes of the 711 clade (i.e., the Arabidopsis MAX1 (Abe et al., 2014), the rice carlactone oxidase (Zhang et al., 2014), which yield canonical, e.g., 4-deoxyorobanchol, and non-canonical, e.g., carlactonoic acid, SLs. Carlactonoic acid is further modified into different products (Alder et al., 2012; Bruno et al., 2014; Al-Babili and Bouwmeester, 2015; Bruno et al., 2017; Abuauf et al., 2018; Jia et al., 2018). ZAS, a recently identified CCD, cleaves apo-10’-zeaxanthinal, yielding the novel signaling molecule, zaxinone (Wang et al., 2019). β-Apo-10’-zeaxanthinal could be formed from zeaxanthin or lutein (not shown) by CCD4 enzymes. Enzymes are surrounded either by ellipses (CCDs) or rectangles (other enzymes). SDR, short chain dehydrogenase reductase; AAO, Abscisic aldehyde oxidase; β-HYD, β-hydroxylase; D27, DWARF27; MAX1, more axillary growth1; OsCO, rice carlactone oxidase, a MAX1 homolog.

Figure 2

Carotenoid derived-hormones and apocarotenoid signaling molecules involved in the establishment of AM symbiosis. Plant roots release SLs which stimulate AMF spore germination, hyphal branching, hyphopodia formation, and metabolism that in the end promote root colonization. Abscisic acid (ABA) deficient mutants show a reduction of AMF colonization and arbuscule formation and functionality (Herrera-Medina et al., 2007; Martín-Rodríguez et al., 2011). However, it is unclear whether ABA effect on the AM symbiosis is mediated by a cross-talk with SLs, ethylene, and gibberellins. Mycorradicins and blumenols are accumulated in arbuscule-containing cells (Walter et al., 2010). Moreover, Wang et al. (2018) demonstrated that blumenols accumulate also in shoots of several mycorrhizal plants and proposed them as foliar markers for a rapid screening of functional AMF associations. Recent findings showed that zaxinone is produced in mycorrhizal roots and a rice zaxinone defective mutant displays lower AM colonization levels (Wang et al., 2019). SP, spore; HP, hyphopodium; IRM, intraradical mycelium; ERM, extraradical mycelium; ARB, arbuscule-containing cells. Note that the specific localization of ABA and zaxinone is not known (indicated with a question mark). Positive and negative effects are illustrated by arrows and blunt-ended bars, respectively.