Floral Volatiles in Parasitic Plants of the Orobanchaceae. Ecological and Taxonomic Implications

Abstract

The holoparasitic broomrapes, Orobanche spp. and Phelipanche spp. (Orobanchaceae), are root parasites that completely depend on a host plant for survival and reproduction. There is considerable controversy on the taxonomy of this biologically and agronomically important family. Flowers of over 25 parasitic Orobanchaceae and a number of close, parasitic and non-parasitic, relatives emitted a complex blend of volatile organic compounds (VOCs), consisting of over 130 VOCs per species. Floral VOC blend-based phylogeny supported the known taxonomy in internal taxonomic grouping of genus and eliminated the uncertainty in some taxonomical groups. Moreover, phylogenetic analysis suggested separation of the broomrapes into two main groups parasitizing annual and perennial hosts, and for the annual hosts, into weedy and non-weedy broomrapes. We conclude that floral VOCs are a significant tool in species identification and possibly even in defining new species and can help to improve controversial taxonomy in the Orobanchaceae.

Keywords: Orobanche; Phelipanche; broomrapes; floral scents; phylogenetic patterns; taxonomy; volatile organic compounds; weeds.

FIGURE 1

Examples of some morphologically, taxonomically, and evolutionary difficult to distinguish broomrape species, (A)Orobanche elatior, (B)Orobanche kochii, (C)Orobanche alsatica, (D)Orobanche mayeri, (E)Phelipanche arenaria, and (F)Phelipanche ramosa.

FIGURE 2

Principal component (PC) analysis of the floral blends of the 32 species studied. Principal component analysis (PCA) was done with compounds showing a significant difference between the species (P < 0.05 from ANOVA test) and it was performed by GeneMath XT. Letters and symbols represent single species. , Antirrhinum majus nanum; , A. majus pumilum; , Boulardia latisquama; , Cistanche phelypea (lutea); , Ci. phelypea (violacea); Cc, Cynomorium coccineum; , Mimulus cardinalis; , M. luteus; Orobanche alba (location 1, 2); , O. alsatica; Ob, O. ballotae (white color); , O. caryophylacea (location 1, 2); , O. cernua; , O. crenata; , O. cumana; , O. elatior; , O. flava (location 1,2,3,4), , O. flava yellow morph (location 1,2,4); , O. foetida; Oh, O. hederae (white color); , O. kochii; , lutea (year 1,2); , O. mayeri; Omi, O. minor (white color); , O. reticulata (location 1,2); , Phelipanche aegyptiaca; , Ph. arenaria; , Ph. mutelii; , Ph. ramosa; , Paulownia tomentosa; , Striga asiatica; , S. gesnerioides; , S. hermonthica.

FIGURE 3

Hierarchical clustering diagram of the flower VOC profiles of 32 species studied. HCA was performed with R and based on PCA of significantly different flower blends. Numbers at nodes are bootstrap probability P-value (BP, upper green numbers) and approximately unbiased P-values (AU, lower red numbers). The definition of the two genera of Orobanche is designated in orange (genus Orobanche) and blue (genus Phelipanche) bar; section Arenariae is also indicated (subsections within genus Orobanche are shown in Figure 6).

FIGURE 4

Hierarchical clustering diagram of the flower VOC profiles of all parasitic plant species studied. HCA was performed with R and it was based on PCA of significantly different flower blends after all non-parasitic plant species where removed from the data set. Numbers at nodes are bootstrap probability P-value (BP, upper green numbers) and approximately unbiased P-values (AU, lower red numbers). The definition of the two genera of Orobanche is designated by orange (genus Orobanche) and blue (genus Phelipanche) bars; section Arenariae is also indicated (subsections within genus Orobanche are shown in Figure 6).

FIGURE 5

Principal component analysis of the floral blends of the 21 European broomrapes studied (including Boulardia latisquama). PCA was done with compounds showing a significant difference between the species (P < 0.05 from ANOVA test) and it was performed by GeneMath XT on a data subset with broomrapes only. Letters and symbols represent single species. Group of wild broomrapes: Orobanche alba (location 1, 2), , O. alsatica; , O. caryophylacea (location 1, 2); , O. elatior; , O. flava (location 1,2,3,4); , O. flava yellow morph (location 1,2,4); Oh, O. hederae (White color); , O. kochii; , O. mayeri; , O. reticulata (location 1,2); , Phelipanche arenaria. Group of weedy broomrapes: Ob, O. ballotae (White color); , O. cernua; , O. crenata; , O. cumana; , O. foetida; , O. lutea (year 1,2); Omi, O. minor (White color); , Ph. aegyptiaca; , Ph. mutelii; , Ph. ramosa. Other broomrapes: , Boulardia latisquama.

FIGURE 6

Hierarchical clustering diagram of the flower VOC profiles of broomrapes of the genus Orobanche. HCA was performed with R and it was based on PCA using a subset with data of Orobanche spp. only. Numbers at nodes are bootstrap probability P-value (BP, upper green numbers) and approximately unbiased P-values (AU, lower red numbers). Internal taxonomic grouping of genus Orobanche as proposed by Teryokhin (1997) is shown by letters and colors which indicate subsections (sections are not specified here), CO, Coerulescentes; CR, Cruentae; GA, Galeatae; GL, Glandulosae; MI, Minores; OR, Orobanche; SP, Speciosae.

FIGURE 7

Hierarchical clustering diagram of the flower VOC profiles of all broomrapes of the genus Phelipanche. HCA was performed with R and it was based on recalculated PCA using a subset with data of Phelipanche spp. only. Numbers at nodes are bootstrap probability P-value (BP, upper green numbers) and approximately unbiased P-values (AU, lower red numbers). Taxonomic grouping of the genus Phelipanche as proposed by Teryokhin (1997) is shown by letters and colors which indicate sections, PP, Phelipanche and PA, Arenariae.