Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions

Abstract

Colonisation of maize roots by arbuscular mycorrhizal (AM) fungi leads to the accumulation of apocarotenoids (cyclohexenone and mycorradicin derivatives). Other root apocarotenoids (strigolactones) are involved in signalling during early steps of the AM symbiosis but also in stimulation of germination of parasitic plant seeds. Both apocarotenoid classes are predicted to originate from cleavage of a carotenoid substrate by a carotenoid cleavage dioxygenase (CCD), but the precursors and cleavage enzymes are unknown. A Zea mays CCD (ZmCCD1) was cloned by RT-PCR and characterised by expression in carotenoid accumulating E. coli strains and analysis of cleavage products using GC-MS. ZmCCD1 eYciently cleaves carotenoids at the 9, 10 position and displays 78% amino acid identity to Arabidopsis thaliana CCD1 having similar properties. ZmCCD1 transcript levels were shown to be elevated upon root colonisation by AM fungi. Mycorrhization led to a decrease in seed germination of the parasitic plant Striga hermonthica as examined in a bioassay. ZmCCD1 is proposed to be involved in cyclohexenone and mycorradicin formation in mycorrhizal maize roots but not in strigolactone formation.

Striga seed-germination activity of root exudates and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced due to root colonization by arbuscular mycorrhizal fungi

“…Our observations confirm and expand previous results with root exudates of mycorrhizal sorghum ) and maize (Sun et al 2008) on germination of S. hermonthica. In our study, we could show that the reduction of seed-stimulating activity due to mycorrhization also occurs in the trap crops cotton and cowpea, which are both false hosts for S. hermonthica.…”

“…Such plants are nonmycorrhizal, while in the field, trap crops can be mycorrhizal. Studies on the tripartite interaction between cereals (sorghum or maize), AM fungi, and S. hermonthica have demonstrated that levels of S. hermonthica seed germination can be significantly reduced with AM root colonization Sun et al 2008). Lower numbers of attached and emerged Striga shoots in the presence of AM fungi have also been reported in laboratory and field studies (Lendzemo and Kuyper 2001;Gworgwor and Weber 2003;Lendzemo et al 2005).…”

“…Although it has been hypothesized that mycorrhization alters root exudation of strigolactones ) and thus reduces the seed-germination activity of root exudates from mycorrhizal plants, no data are available yet on the nature of the alteration which is responsible for the altered effect of root exudates from mycorrhizal and nonmycorrhizal plants on the seed germination of Striga plants Sun et al 2008). Recently, by mixing pea root exudates with a solution of the synthetic strigolactone analog GR-24, it could be shown that a lower seed-germination activity of the root exudates of rhizobial pea plants on Orobanche is at least partially due to the presence of seed germination inhibitors in those exudates (Mabrouk et al 2007).…”

RNA Interference-Mediated Repression of MtCCD1 in Mycorrhizal Roots of Medicago truncatula Causes Accumulation of C27 Apocarotenoids, Shedding Light on the Functional Role of CCD1

“…S1). This indicates that MtCCD1 belongs to the well-studied class of CCD1 proteins and genes (Schwartz et al, 2001;Simkin et al, 2004aSimkin et al, , 2004bMathieu et al, 2005;Auldridge et al, 2006a;Ibdah et al, 2006;Kato et al, 2006;Sun et al, 2008;Vogel et al, 2008;Supplemental Fig. S1).…”

Soil Maize Cultivar-related Challenges on Striga hermonthica Infested Fields in Western Kenya

“…This has been raising research interests, especially the relationship between carotenoid expression in yellow maize and the exudation of strigolactones that stimulate the germination of S. hermonthica seeds (Matusova et al, 2005;Li, Vallabhaneni, Yu, Rocheford, & Wurtzel, 2008;Jamil, Charnikhova, Verstappen, & Bouwmeester, 2010;Jamil, Kanampiu, Karaya, Charnikhova, & Bouwmeester, 2012). Greater carotenoid expression with concomitant low rate of carotenoid cleavage is suspected to prevent the exudation of carotenoid-derived germination factors for S. hermonthica, particularly strigolactones (Matusova et al, 2005;Sun et al, 2008;Floss & Walter, 2009). Besides, carotenes in yellow maize are important in human nutrition as a source of pro-vitamin A (Hwang et al, 2016).…”