Broomrape infestation in carrot (Daucus carota): Changes in carotenoid gene expression and carotenoid accumulation in the parasitic weed Phelipanche aegyptiaca and its host

Abstract

carotenogenesis has been intensively studied in carrot roots, and transcriptional regulation is thought to be the major factor in carotenoid accumulation in these organs. However, little is known about the transcriptional regulation of carotenoid biosynthetic genes concerning carotenoid accumulation during infestation by the obligate parasite Phelipanche aegyptiaca. HpLc analysis revealed a decrease in carotenoid levels of the different carrot cultivars when parasitized by P. aegyptiaca. Besides, we isolated and analyzed P. aegyptiaca tubercles parasitizing the various carrot root cultivars and show that they accumulate different carotenoids compared to those in non-infested carrot roots. expression analysis of PHYTOENE SYNTHASE (PSY1) and CAROTENOID ISOMERASE (CRTISO) as well as the strigolactone apocarotenoid biosynthetic genes DWARF27 (D27), CAROTENOID CLEAVAGE DIOXYGENASE 7 (CCD7) and CCD8 revealed that their transcript levels showed significant variation in P. aegyptiaca infested carrot roots. After parasite infestation, the expression of these genes was strongly reduced, as were the carotenoid levels and this was more pronounced in the uncommon non-orange varieties. We also analyzed the parasite genes encoding D27, CCD7 and CCD8 and show that they are expressed in tubercles. this raises important questions of whether the parasite produces its carotenoids and apocarotenoids including strigolactones and whether the latter might have a role in tubercle development. The parasitic weeds of the genera Orobanche, Phelipanche, and Striga (Orobanchaceae) are the most important agricultural weeds in many crops, particularly in carrot, tomato, sunflower, tobacco, and faba bean, causing significant crop losses in many parts of the world 1. These obligate root parasites are completely devoid of chlorophyll and consequently dependent on their host for supply of resources, including water, nutrients, proteins, and oligonucleotides 2-5. The parasite development is divided into pre-parasitic and parasitic stages. The pre-parasitic stage starts with seed pre-conditioning followed by germination. The parasite seed germination is induced by molecules secreted into the rhizosphere by the roots of host plants called germination stimulant 6. Germination stimulants for root parasitic plants have been isolated from host plant root exudates, and the majority of these natural compounds are carotenoid-derived strigolactones 7,8. The parasitic phase begins with the penetration of the parasite haustorium connecting to the host vascular tissues. The haustoria are responsible for host attachment, penetration and resource acquisition 9. The parasite first develops a tubercle, which gives rise to a flowering spike that emerges from the soil 9-12. The flower produces thousands of extremely small seeds, which can survive more than 15 years in a crop field until favorable environmental conditions for germination are obtained 4,9-12 .

The Effect of 10 Crop Plants That Served as Hosts on the Primary Metabolic Profile of the Parasitic Plant Phelipanche aegyptiaca

“…Second, the observation that several compounds that inhibit enzymes in amino acid biosynthetic pathways are able to kill broomrape [15,16] suggests that these enzymes are active in the parasite. Third, the parasite can form its own carotenoids, as recently reported [17].…”

Biosynthesis and apoplast accumulation of the apocarotenoid pigment azafrin in parasitizing roots of Escobedia grandiflora

“…This might not be a general trend in parasitic plants. For example, the tubercle of the holoparasitic plant Phelipanche aegyptiaca showed a high expression of D27, CCD7, and CCD8 when parasitizing the host roots (Emran et al ., 2020). However, mycorrhizal plants that produce high levels of apocarotenoids reduce their production and secretion of SL, likely because abundant apocarotenoid production in AM-colonized roots might generate a metabolic sink and successfully compete for SL precursors (Walter et al ., 2010).…”

Accumulation of azafrin in the root apoplast of the medicinal plant Escobedia grandiflora might play a role in parasitism

“…For example, the tubercle of the holoparasitic plant Phelipanche aegyptiaca (Pers.) Pomel showed a high expression of D27, CCD7, and CCD8 when parasitizing the host roots (Emran et al, 2020). However, mycorrhizal plants that produce high levels of apocarotenoids reduce their production and secretion of SL, likely because abundant apocarotenoid production in AM-colonized roots might generate a metabolic sink and successfully compete for SL precursors (Walter et al, 2010).…”