![Orobanche cumana A, plant in its habitat along with host; B, loosely held (distant) flowers; C, host plant Artemisia japonica with parasite Orobanche cumana showing root connection. [Images by Ashutosh Sharma]](https://www.researchgate.net/profile/Ashutosh-Sharma-45/publication/352777046/figure/fig1/AS:1039172068462592@1624769336406/Orobanche-cumana-A-plant-in-its-habitat-along-with-host-B-loosely-held-distant_Q320.jpg)
![Orobanche cumana in situ A, bract and calyx, 1-bract, 6 & 7-calyx lobes, 2 & 4-anterolateral segments of calyx lobes, 3 & 5-posterolateral segments of calyx lobes, 8-point of attachment with stem; B, pollinator Ceratina simillima visiting the flower; C, plant in its habitat, with non-host Artemisia vestita growing in proximity on right side and its young host plant of A. japonica on left side (indicated by arrow). [Images by Ashutosh Sharma]](https://www.researchgate.net/profile/Ashutosh-Sharma-45/publication/352777046/figure/fig2/AS:1039172068442112@1624769336483/Orobanche-cumana-in-situ-A-bract-and-calyx-1-bract-6-7-calyx-lobes-2_Q320.jpg)
Content uploaded by Ashutosh Sharma
Author content
All content in this area was uploaded by Ashutosh Sharma on Jun 27, 2021
Content may be subject to copyright.
Orobanche cumana (Orobanchaceae), an addition
to the flora of India from Himachal Pradesh
(Western Himalaya) with a new host record
Ashutosh Sharma1*, Nidhan Singh2, D.S. Rawat3 & Som Dutt Sharma4
________________________________
1. The University of Trans-Disciplinary Health Sciences and Technology (TDU), Post Attur via
Yelahanka, Bengaluru-560064, Karnataka, India.
2. I.B. (PG) College, Panipat-132103, Haryana, India.
3. Department of Biological Sciences, College of Basic Sciences & Humanities, G.B. Pant
University of Agriculture and Technology, Pantnagar-263145, Uttarakhand, India.
4. College of Horticulture & Forestry (Dr. Yashwant Singh Parmar University of Horticulture
and Forestry) Neri, Hamirpur-177001, Himachal Pradesh, India.
* author for correspondence: ashutoshsharma11sn@gmail.com
________________________________
Abstract
Wallroth, collected from lower Kullu Valley of Himachal
Pradesh in Western Himalaya, is reported here as a new record for the flora
of India with Thunberg as a host recorded for the first
time. This is a distinct species widely distributed from Eastern Europe to
Siberia and Western and Northern China but yet unreported from India.
The species belongs to Linnaeus section (Beck) Rouy
series Novopokrovskij and is very closely related to
Linnaeus from which it differs by a combination of characters: longer, lax
inflorescence, smaller flowers held distantly on scape, and host range. The
detailed description, photographs, discussion/comments on confusion with
related taxa, ecology and pollination of the species are also provided.
Manuscrit reçu le 02/06/2021 Article mis en ligne le 25/06/2021 – pp. 189-205
Résumé
Wallroth a été collecté dans la basse vallée de Kullu de
l'Himachal Pradesh dans l'Himalaya occidental, ce qui constitue une
addition à la flore de l'Inde. C'est également la première fois que
Thunberg est observé comme hôte. Il s'agit d'une espèce distincte
largement distribuée depuis l'est de l'Europe jusqu'en Sibérie et à l'ouest et
au nord de la Chine, mais non encore signalée en Inde. L'espèce appartient
à Linnaeus section (Beck) Rouy série
Novopokrovskij et est très étroitement apparentée à Linnaeus
dont elle diffère par une combinaison de caractères : inflorescence plus
longue et lâche, fleurs plus petites distantes l'une de l'autre sur la hampe et
type d'hôtes. Une description détaillée de l'espèce, accompagnée de
photographies, une discussions relative à la confusion avec les taxons
apparentés, des données sur son écologie et sa pollinisation sont proposées.
Keywords: , holoparasitic plant, Kullu valley, parasite,
taxonomy.
Mots clés : , parasite, plante holoparasitaire, taxinomie,
vallée de Kullu.
Introduction
Linnaeus (1753: 632) is a morphologically complex genus of
holoparasitic plants comprising 160-180 species worldwide, the majority of
them being distributed in temperate and subtropical regions across the
northern hemisphere of old world (Mabberley, 2017; POWO, 2019; WCVP,
2020). The updated Index of Orobanchaceae (Sanchez Pedraja ., 2016)
lists 119 species of [excluding 64 species of Pomel
(1874: 102)]. The members of the genus are achlorophyllous, leafless, root
parasitic herbs and some of them are restricted to particular host families.
For nutrition, they completely depend on their host plants and get food by
establishing direct contact with host roots. Hooker (1884) described 11
species of in British India. Presently, the genus is represented by
13 species in India (Anilkumar, 2000), all of which are distributed in
Western Himalaya. Based on the phytogeography of in India,
Western Himalaya clearly stands out as the richest phytogeographical
zone. Wallroth (1825: 58) described , based on plants
collected by Marschall von Bieberstein in Volga area (Astrakhan desert),
190
SW Russia but Beck (1930) considered this species as a variety of
Linnaeus in Loefling (1758: 152) ( var. ) and reported
central Asia to South-eastern Europe as the main distribution area.
Originally, was known to parasitize exclusively spp.
(Venkov & Bozoukov, 1994) in the wild but after the introduction and large
scale cultivation of sunflower ( Linnaeus, 1753: 904) in
Russia, plants of were detected for the first time parasitizing this
crop in Voronev in 1866 (Morozov, 1947). In the 20th century this species
spread to many other European and Western Asian Countries and become
a serious parasitic weed of mainly (but not limited to) sunflower crop and
this variety affecting crops is now called as var. Tzvelev
(2015: 214) which is actually different from the type species. We report here
first confirmed record of for the Indian flora based on the
specimens collected from wild habitat and exclusively parasitizing
Thunberg (1784: 310) which itself is a new host record for
any species.
Material and Methods
The first author has been exploring plant diversity of Himachal Pradesh,
India, for the last four years and, during a routine plant exploration in
lower Kullu valley of Himachal Pradesh, he came across a small population
of an interesting sp. parasitizing exclusively
(Fig. 1). Identification of these specimens through consultation of herbaria
of BSD, DD, CAL, GUH and relevant local literature (Collett, 1921;
Chowdhery & Wadhwa, 1984; Polunin & Stainton, 1984; Stainton, 1988;
Aswal & Mehrotra, 1994; Dhaliwal & Sharma, 1999; Singh & Rawat, 2000;
Srivastava & Shukla, 2015; Singh, 2018), account of the genus in
(Hooker, 1885), revision of the family Orobanchaceae in India
(Anilkumar, 2000), and account of the genus in floras of adjacent countries
(Schiman-Czeika, 1964; Jafri, 1976; Zhang & Tzvelev, 1998; Press ., 2000)
was not successful. These specimens were finally determined as
with the help of Dr. Óscar Sánchez Pedraja (GBC, Liérganes, Spain).
This species, known to be distributed in Central Asia to South-eastern
Europe, was not yet reported from India. Hence, these specimens are
described here with images of live plants, new host record and associated
information.
in India– A. Sharma
Figure 1. Orobanche cumana
A, plant in its habitat along with host; B, loosely held (distant) flowers; C, host plant
with parasite showing root connection.
[Images by Ashutosh Sharma]
192
Taxonomic account
Orobanche cumana Wallroth, !"
##$%: 58 (1825).
Plants annual or biennial, total root parasite, achlorophyllous. Stem
slender, thin, 15-45 cm long, unbranched, up to 1 cm in diameter at base,
purplish with brown streaks at base, completely covered with glandular
trichomes. Rhizomes highly variable in shape and size, covered with
yellowish/brown scales, establishing connection with a thin root of the
host. Roots shallow, clustered and rudimentary. Leaves reduced to scales,
alternate, limited to the axis below the flowers, pale purple to yellow,
turning into brown, 4-5 × 8-10 mm, ovate, acute to minutely acuminate, tips
dry down and wither soon. Inflorescence racemose, spicate, 10-25 cm long,
consisting of 12-30 sessile flowers, arranged spirally in acropetal
succession, ca. 1-2 cm distant at base, inter-flower distance gradually
decreasing towards apex. Bracts as long as or slightly longer than calyx but
always shorter than corolla tube, 4-5 × 8-10 mm, similar in shape and size to
scales, persistent; bracteoles absent. Flowers sessile, purplish, 14-18 mm
long. Calyx adaxially covered with glandular trichomes including the
edges, deeply 2-lobed, lobes lateral, separation reaching the base, 7-9 mm
long, each lobe bipartite, segments unequal and variable, smaller segment
anterolateral, 2-3 mm long, ca. 1 mm wide, thinner, partly or entirely
concealed beneath the bract, larger segment posterolateral, 3-5 mm long,
free from bract. Corolla tubular, dark purple, 14-18 mm long, slightly
curved, slightly constricted above insertion of filaments, glandular hairy
outside, 5-lobed, lobes nearly equal, curved outwards, margins irregularly
dentate, inter-lobal distance between posterior pair slightly shorter than the
distance between the three anterior lobes. Stamens 4, epipetalous, dark
yellow colour prominent at the junction of filament and corolla, partially
didynamous, posterior pair inserted on corolla tube ca. 1-2 mm lower than
anterior pair; filaments ca 8 mm long, nearly glabrous at base and
minutely pubescent towards apex, inserted at 5-6 mm above the base of
corolla tube, curved inwards near the apex, thus positioning anthers facing
each other; thecae equal, parallel, both fertile, more pubescent at
sutures/openings, mucronate at base. Pistil ca. 13 mm long; ovary oblong or
ovoid, 7-8 mm long, glabrous, unilocular with 4 parietal placentae; style
curved just below the stigma, ca 7 mm long, persistent; stigma bilobed,
covered with minute glandular trichomes, white. Fruit an unilocular
in India– A. Sharma
capsule, ca 10 mm long, glabrous, laterally dehiscent. Seeds numerous,
minute, oblongoid, dark brown, ca. 0.3 mm long, nearly half as broad as
long (Fig. 2).
can be separated from its close relative by its long, lax
inflorescence, smaller flowers placed distantly on scape (at least at base)
and its host range. This species has unbranched stem, distinctly lacks
bracteoles, flowers are sessile, calyx is incised into 2 lateral lobes which are
further 2-partite. The characters like corolla with elongated tube usually
more or less inflated below the place of insertion of the stamens, slightly
narrowed and then again spreading upwards, insertion of stamens at
corolla tube one-third from base or above, indicate its position in
sect. (Beck) Rouy (1909: 167) [≡ subsection Beck
(1882: 124)]. Complementary characters such as plant glandular-pubescent,
parasitic on Asteraceae members, corolla tube strongly curved forward,
with distinct constriction above the place of insertion of the stamens,
somewhat below the middle of corolla tube, sub-glabrous anthers, clearly
indicate its position in series Novopokrovskij (1930: 314).
Ecology and distribution: was collected at 1100-1200
meters a.s.l. from Jhiri village area, lower Kullu Valley (Mandi district) of
Himachal Pradesh which lies between Pir Panjal and Dhauladhar
mountain ranges. The individuals of this species were found growing on
exposed, rocky pastures, dominated by &(Linnaeus, 1759:
878) Palisot Beauvois (1812: 165), '(Ledebour, 1815: 515)
Schultes (1824: 345), ( Linnaeus (1753: 775), #
Bentham (1834: 378), ( ) Bentham (1846: 510),
Thunberg (1780: 209), ) Wallich ex Besser (1834:
25), * (Charles Baron Clarke, 1876: 162) Pampanini (1926: 452)
andWaldstein & Kitaibel (1801: 66).
Specimens examined: INDIA, Himachal Pradesh, Mandi District (Kullu
Valley), Jhiri, on dry species-rich hilly pastureland, 31°83’24” N,
77°16’53” E, 1150 m a.s.l., 14 April 2020, Ashutosh Sharma,(+++++,-.,/0
(+++++,-.,10(+++++,-.,-0(+++++,-.,203(4.,-+5
Accessed online: INDIA, Cachemire:
P 02968095 http://mediaphoto.mnhn.fr/media/1441353151109AvL9SS1y3K38nTqd,
P 02968090 http://mediaphoto.mnhn.fr/media/1441353151012Nzadu6r6oIBysKfu,
194
Figure 2. Orobanche cumana
A, inflorescence; B, shoot emerging from rhizome with intact host root connection; C, a part of
scape; D, stem showing glandular trichomes; E, bract/scale; F, flower side view; G, flower
front view; H, calyx; I, corolla exterior; J, corolla interior; K, corolla spread open; L, stamen
attached to corolla tube; M, pistil; N, mature capsule; O, ovary (transverse section); P, seeds.
[Images by Ashutosh Sharma.]
in India– A. Sharma
Coimbatore, Tamil Nadu:
K 000061383 http://specimens.kew.org/herbarium/K000061383
K 000061384 http://specimens.kew.org/herbarium/K000061384
RUSSIA, Old Sarpeta:
P 02968103 https://mediaphoto.mnhn.fr/media/14413531512615OWFuwo01cLAQHTC
P 04410446 https://mediaphoto.mnhn.fr/media/1441359764088E2Avf8x7ni3fS1sZ
COI 00056874 https://coicatalogue.uc.pt/index.php?t=specimen&COINumber=56874
Host: belongs to series , where members are
parasitic usually on members of Asteraceae (Novopokrovskij and Tzvelev,
1958). In the wild, is mostly found growing on several
species and the first reports of parasitizing on sunflower came
from Voronev, Russia in 1866 (Morozov, 1947). In 20th century, this species
reached agricultural fields in several parts of Europe and Asia where it is
reported parasitic on various cultivated plants e.g., Sunflower (
), Tomato (6 & Linnaeus, 1753: 185), Aubergine
(6 * Linnaeus, 1753: 186) and Tobacco (7
Linnaeus, 1753: 180) (Novopokrovskij & Tzvelev, 1958; Labrousse 8 2001;
Piwowarczyk 8 2019). But interestingly, our recently discovered
population of has been found to be precisely host-specific in
nature with the host invariably being . Repeated and
careful observations of the population revealed that in spite of presence of
three more species, viz. ), *, and in
the same locality and soil, it has been seen to establish connection with the
roots of its specific host () only (Fig. 3). Further, it is noteworthy
that its confirmed host species, 8 has not been recorded as host of
any species till now (Sánchez Pedraja ., 2016).
Flowering/fruiting and pollination: Flowering is recorded from early
April to May, gradually followed by fruiting from late April to late May.
Pollination is done by a couple of species of small Carpenter Bees,
particularly by Smith, characterised by having
pubescence on head and legs, which helps it in carrying pollen. It is one of
the few pollinators visiting its flowers, because large insects are not able to
enter the flowers, the mouth of which is smaller (less than 5 mm) than
many other potential pollinators.
196
Figure 3. Orobanche cumana in situ
A, bract and calyx, 1-bract, 6 & 7-calyx lobes, 2 & 4-anterolateral segments of calyx lobes, 3
& 5-posterolateral segments of calyx lobes, 8-point of attachment with stem;
B, pollinator visiting the flower; C, plant in its habitat, with non-host
)growing in proximity on right side and its young host plant of
on left side (indicated by arrow). [Images by Ashutosh Sharma]
in India– A. Sharma
Identity confusion with Orobanche cernua
was described based on materials collected by Pehr
Löfling (Loefling) near Aranjuez, central Spain. It parasitizes different
species of the Asteraceae, being most frequently found on plants of the
genus in the wild much like which itself is a
polymorphous species, very closely allied to , although the
differences between these two species cannot always be easily expressed
(Novopokrovskij & Tzvelev, 1958; Tzvelev, 1981; Pujadas & Velasco, 2000).
The populations attacking sunflower seem to be unable to
attack tobacco and ) ) (Musselman, 1994) so, according to some
authors, they should be taxonomically distinguished either as separate
subspecies or as two species, indicating the sunflower broomrape as
(Dhanapal 1996: 10, sub ). So was
earlier considered a subspecies of , until Joel (1988), Jacobsohn
. (1991) and Paran . (1997) clearly differentiated two species on the
basis of morphological and host range differences; later this separation was
also supported by seed-oil fatty acid profiles (Pujadas & Thalouarn, 1998;
Pujadas-Salvà & Velasco, 2000), seed morphology (Plaza ., 2004) and at
the molecular level (Román ., 2003; Pineda-Martos ., 2014). These
two species can be distinguished when comparing typical specimens (e.g.,
when comparing specimens of growing on cultivated plants) but
this is not easy when the specimens are less typical. On the other hand, the
staminal indumentum is variable (glabrous/hairy) and may be of no value in
differentiating the two taxa (e.g., from has hairy
stamens) as some authors think (Novopokrovskij & Tzvelev, 1958; Tzvelev,
1981). The form of “ subsp. 9 parasitizing sunflower is the
result of anthropogenic activity, which, in any case, cannot be considered
as the typical subspecies (Tzvelev, 1981).
The most important differentiating character between both taxa is the size
of the corolla. It is smaller in length and diameter in . Other
characters, such as the number of flowers or the density of the
inflorescence, are sometimes quite variable and have led to the description
of numerous forms. However, in general is a more graceful herb
having less dense inflorescence, with fewer flowers than
(Novopokrovskij & Tzvelev,1958).
The comparison between and by Pujadas-Salvà and
Velasco (2000) in the Iberian Peninsula is actually between
198
and var. and not the typical wild . The same
is true of Joel (1988), Jacobsohn . (1991) and Paran (1997), as they
compared that parasitizes tomato (as ) with the one that
parasitizes sunflower (as ). Additionally, they do not compare
the types of both taxa in Spain and Russia respectively. In our opinion, the
ratio between the length of the corolla and the width of the corolla on the
throat is smaller in along with lax inflorescence and lesser
number of flowers in wild population. These measures may be more
convincing, if they are done on the individuals from their own locality, and
specifically those which are parasitizing wild species rather than crop
plants, like var. .
Discussion and conclusion
is a complicated genus, on account of complex morphology
(owing to intraspecific variations), short reproductive phase, reduced
vegetative parts and also the non-preservation of distinguishing characters
while preparing herbarium material. The specimens quickly lose important
characteristics like colour and shape of corolla etc. during preservation
(Anilkumar, 2000). Due to these factors, Indian herbaria lack good and
correctly identified specimens of the genus. A thorough study of this genus
in India, based on live material as well as herbarium specimens is much
needed. Some of the Indian species are very little known, as for instance
C.B. Clarke ex Hooker(1884: 324) is not even represented in
any Indian herbarium and is only known by its type at K
(http://specimens.kew.org/herbarium/K000061388 Digital Image).
In the past, most of the studies dealing with have been done on
the plants that parasitize sunflower, i.e. var. and not on
true specimens of collected from (Astrakhan
desert, Russia). In Europe, var. is the only species that
attacks several crops and we think the same may be true in India, along
with *& (Persoon) Pomel (1874: 107) (= *&
Persoon, 1806: 181) which is another major crop-infesting species in India.
So further field work is needed to inspect and reconfirm identities of what
is known as affecting tobacco and few other agricultural crops in
India. There are reports of [] parasitizing tobacco
plants according to Becker’s collection (COI 00056874)
https://coicatalogue.uc.pt/index.php?t=specimen&COINumber=56874 so
in India– A. Sharma
there are good possibilities that even the forms that parasitize tobacco and
other Solanaceae species in India would be included in
[ Wight (1850: 179) and subsp.
Teryokhin (1996: 246)]. Also, as we examined online specimens from India
by accessing the data available on Index of Orobanchaceae (Sánchez
Pedraja ., 2016 onwards), we found an interesting specimen from
Kashmir (P02968095) (Chagnoux, 2021) identified as that
looks near similar to our plant specimens. As this locality is from
neighbouring union territory, this gives more evidence that true wild
occurring population of may be more widespread in Western
Himalayan region. However, other specimens from India given in this
database (particularly from South India and growing on crops) having
much dense inflorescence with very high number of flowers, thick and
often branched scapes need further detailed work and field analysis to
confirm their true identity, which otherwise is not possible to confirm from
merely herbarium specimens.
By perusal of literature related to Indian species of this genus, it has been
reflected that the specific identification of the host has not been given due
priority. Consequently, the hosts of many of the Indian spp. are
known only at the genus level, like spp. However, a recent study
(Schneider 8 2016) has suggested that host specificity and host
switching are important drivers of speciation in Therefore, it is
opined here that future collections and studies of this genus must also
include species identification of the host plants. Knowing the exact host
species will lead to better understanding of complexes like and
such findings may even invoke discoveries of new cryptic taxa.
Acknowledgements
The authors are grateful to Dr. Óscar Sánchez Pedraja (GBC, Liérganes,
Spain) and Dr. Renata Piwowarczyk (UJK, Poland) for their highly valuable
comments and discussion helping in refining the manuscript. We are also
thankful to the Scientist-In-charge, CAL and Dr. Gopal Krishna, CAL for
their genuine support in deposition of voucher material of the plant. First
author is highly grateful to his father, Sh. Pawan Kumar Sharma for his
regular help in field explorations.
200
References
Anilkumar, R., 2000. :;3) &
Ph.D. Thesis, Bharathiar University, India (Available from
http://hdl.handle.net/10603/105458,)
Aswal, B.S. & B.N. Mehrotra, 1994. (<6=
7%&>. Bishen Singh Mahendra Pal Singh, Dehradun, India.
pp. 496–498.
Beck von Mannagetta, G., 1882. 7?*!)7<
Wien, 124 pp.
Beck von Mannagetta, G., 1930. Orobanchaceae.$Engler, A. (Ed.),
! IV: 261. Wilhelm Engelmann, Leipzig, 348 pp.
Bentham, G., 1834. (6. J. Ridgway & sons, London,
378 pp.
Bentham, G., 1846. 6&73*@* [A. P. de
Candolle] 10: 510.
Besser, W.G. [W.S.J.G.], 1834. 7);#A6AAA
7# 3: 25.
Chagnoux, S., 2021. The vascular plants collection (P) at the Herbarium of
the Muséum national d'Histoire Naturelle (MNHN - Paris). Version 69.194.
MNHN - Muséum national d'Histoire naturelle. Occurrence dataset
https://doi.org/10.15468/nc6rxy accessed via GBIF.org on 2021-01-20.
Chowdhery, H.J. & B.M. Wadhwa, 1984. Orobanchaceae. $ Chowdhery,
H.J. & Wadhwa, B.M. (Eds.), $ &: 540-541.
BSI, Howrah.
Clarke, C.B., 1876. 6
. Calcutta, Bombay, London. 162pp.
Clarke, C.B., 1884. . : Hooker, J.D.,
volume IV part XI: 324. L. Reeve & Co., London.
Collett, H., 1921. 6. Thacker Spinc & Co, London. Reprint ed.
1971, Bishen Singh Mahendra Pal Singh, Dehradun, India.
Dhaliwal, D.S. & M. Sharma, 1999. '=>.
Bishen Singh Mahendra Pal Singh, Dehradun, India. 744 pp.
Dhanapal, G.N., 1996. #*=(>
=7 (> Doctoral thesis, Wageningen Agricultural
University, Wageningen, The Netherlands, 183 pp.
Hooker, J.D., 1884. Orobanchaceae. : Hooker, J.D. (Ed.)
volume IV part XI: 319-328. L. Reeve & Co., London. DOI:
https://doi.org/10.5962/bhl.title.678.
in India– A. Sharma
Jacobsohn, R., B. Bohlinger, E. Eldar & V.P. Agrawal, 1991. Crop host range
of species in an experimental field. In: Ransom, J. K., Musselman,
L. J., Worsham, A. D. and Parker, C. (eds), 6&
%, Nairobi, Kenya, 24-30 June 1991, pp. 176-179.
Jafri, S.M.H., 1976. Orobanchaceae. : E. Nasir & S. I. Ali (Eds.)
98 (4): 1–23. Karachi. (http://legacy.tropicos.org/Name/40033763?
projectid=32; accessed several times).
Joel, D., 1988. - A new adventive weed in Israel.
& 16: 375.
Labrousse, P., M.C. Arnaud, H. Serieys, A. Bervillé & P. Thalouarn, 2001.
Several mechanisms are involved in resistance of to
Wallr. & 88: 859-868. DOI: https://doi.org/
10.1006/anbo.2001.1520.
Ledebour, C.F., 1815. #A B 6 6
*)BBe 5: 515. St. Petersburg.
Linnaeus, C., 1753. 6.
Linnaeus, C., 1759. 6&78C2: 878
Loefling, P., 1758. 8:?C
8D?EF4-/4F4-/18*DD)
?)?* )?;8 *) C E? (.
Stockholm: Ttryckt på Direct. Lars Salvii Kostnad.
Mabberley, D.J., 2017. #&G<<&8
. Cambridge University Press, Cambridge, UK. 1102pp.
Morozov, V.K., 1947. Sunflower breeding in USSR. ! 274.
Moscow. (in Russian).
Musselman, L.J., 1994. Taxonomy and spread of Orobanche. In: Pieterse,
A.H., Verkleij, J.A.C., Borg, S.J. ter (eds.). *&#*:
27-35. Proceedings of the international workshop on and related
6* research (3rd: 1993: Amsterdam). Amsterdam: Royal Tropical Institute.
Novopokrovskij, I.V., 1930. #& & *
@(')76663. Leningrad 13: 314.
Novopokrovskij, I.V. & N.N. Tzvelev, 1958. Orobanchaceae. In: Shishkin, B.K.
(ed.). H366)=H366>, vol.
23: 685-687. Institutum Botanicumnomine V. L. Komarovii Academiae
Scientiarum URSS, Mosqua and Leningrad.
Palisot de Beauvois, A. M. F. J., 1812 CB)**88
IJKLMNKOPQMRSMTPUMTPQSNVWRXMTPYPNLMZP[QKSMTPSM\SXTMR]NR]P^MTPZNSNZ]_SMTPUMP]JKT
*8 t.5: 165. Chez l'auteur, Paris.
202
Pampanini, R., 1926. 7)06
8 Ser.2, 33: 452. Florence.
Paran, I., D. Gidoni & R. Jacobsohn, 1997. Variation between and within
broomrape () species revealed by RAPD markers. &78: 68-
74.
Persoon, C.H., 1806. 6& $ C 8
&`* 2(1):
181. Parisiis Lutetiorum.
Pineda-Martos, R., L. Velasco, A.J. Pujadas-Salvà, J.M. Fernández-Martínez
& B. Pérez-Vich, 2014. Phylogenetic relationships and genetic diversity
among Wallr. and L. (Orobanchaceae)
populations in the Iberian Peninsula 7 (61): 161-171.
Piwowarczyk, R., Ó. Sánchez Pedraja, G. Moreno Moral, G. Fayvush,
N. Zakaryan, N. Kartashyan & A. Aleksanyan, 2019. Holoparasitic
Orobanchaceae (, &, , ) in Armenia:
distribution, habitats, host range and taxonomic problems. &; 386(1):
001-106.
Plaza, L., I. Fernandez, R. Juan, J. Pastor & A.J. Pujadas Salvà, 2004.
Micromorphological studies on seeds of Orobanche species from the
Iberian Peninsula and the Balearic Islands, and their systematic
significance& 94: 167-178.
Polunin, O. & A. Stainton, 1984. a&. Oxford University
Press, New Delhi. 305 pp.
Pomel, A.N., 1874. 7);A;` 11. Paris, 399 pp.
POWO, 2019. “%”. Facilitated by the Royal Botanical
Gardens, Kew. Published at http://plantsoftheworldonline.org/ Retrieved
05 June 2020.
Press, J.R., K.K. Shrestha & D.A. Sutton, 2000.
a*7. The Natural History Museum, London. Updated
version available from: www.eFloras.org (Accessed: several times).
Pujadas, A. & P. Thalouarn, 1998 Loefl. &
Wallr. in the Iberian Peninsula. *1#6&
C%36: 159-160.
Pujadas-Salvà, A.J. & L. Velasco, 2000. Comparative studies on
L. and Wallr. (Orobanchaceae) in the Iberian Peninsula.
b ( 6& 134(4): 513-527. DOI:
https://doi.org/10.1006/bojl.2000.0346.
in India– A. Sharma
Román, B., C. Alfaro, A.M. Torres, M.T. Moreno, Z. Satovic, A. Pujadas &
D. Rubiales, 2003. Genetic relationships among Orobanche species as
revealed by RAPD analysis. & 91: 637-642.
Rouy, G., 1909. $ 8 `
A 8 <( c 3& b
"d=6> 11: 167.
Sánchez Pedraja, Ó., G. Moreno Moral, L. Carlon, R. Piwowarczyk, M. Lainz
& G.M. Schneeweiss, 2016. [continuously updated]. Index of Orobanchaceae.
http://www.farmalierganes.com/Otrospdf/publica/Orobanchaceae
%20Index.htm. Liérganes, Cantabria, Spain. ISSN: 2386-9666
Schiman-Czeika, H., 1964. . $K. H. Rechinger (Ed.),
5: 2-20. Akademische Druck- und Verlagsanstalt- Graz.
Schneider, A.C., A.E. Colwell, G.M. Schneeweiss & B.G. Baldwin, 2016.
Cryptic host-specific diversity among western hemisphere broomrapes
(Orobanches.l., Orobanchaceae). & 118(6): 1101-1111.
DOI:10.1093/aob/mcw158
Schultes, J.A., 1824. #@66&@*
(;Cbb3. 345 pp.
Singh, P.B., 2018. # $ 7 %
&. Bishen Singh Mahendra Pal Singh, Dehradun, India.
Singh, S.K. & G.S. Rawat, 2000. & 7 8
. Bishen Singh Mahendra Pal Singh, Dehradun, India. 304 pp.
Srivastava, S.K. & A.N. Shukla, 2015. %&8
8 Volume 2. BSI, Kolkata.
Stainton, A., 1988. a&$6. Oxford University
Press, New Delhi. 46 pp.
Teryokhin, E.S. & S.I. Chubarov, 1996. Two modes of the vegetative
propagation in Orobanche cernua (Orobanchaceae). )
: 243-248. 6 th International Parasitic Weed Symposium, Junta
de Andalucía, Spain.
Thunberg, C.P., 17807)3*66H3:
209.
Thunberg, C.P., 1784. b :
310.
Tzvelev, N.N., 1981. Orobanchaceae Vent. : Fedorov, A.A. (ed.),
C)6663 [Flora of Russia: The European Part and Bordering
Regions] Vol. 5: 434-461. Nauka; Leningrad.
204
Tzvelev, N.N., 2015. O rode zarazikha (Orobanche L. sensu lato,
Orobanchaceae) v Rossii [On the genus Orobanche L. sensu lato
(Orobanchaceae) in Russia]. 7)6@&3 46: 189-215.
Venkov, V. & H. Bozoukov, 1994. Influence of different species of
on cultivated sunflower and tobacco. In: A.H. Pieterse, J.A.C.
Verkleij and S.J. Ter-Borg (eds.), *&#*: 349-
350. Proc. 3rd Int. Workshop on and related 6* Research.
Royal Tropical Institute, Amsterdam, The Netherlands.
Waldstein, F.P.A. & P. Kitaibel, 1801.
3*1: 66, t. 65.
Wallroth, K.F.W., 1825. *$
#, 80 pp.
WCVP, 2020. %@s, version 2.0. Facilitated by
the Royal Botanic Gardens, Kew. Available from:
http://wcvp.science.kew.org/ (Accessed: 04 June 2020).
Wight, R., 1850. Illustrations of Indian Botany; or Figures Illustrative of
each of the Natural Orders of Indian Plants, described in the author's
Prodromus Florae Peninsulae Indiae Orientalis. Vol. 2. Madras. [CIX.
Orobanchaceae: 176-180].
Zhang, J-Y & N.N. Tzvelev, 1998. Orobanchaceae. $Zhengyi, W., Raven,
P.H. & Deyuan, H. (Eds.), Flora of China 18: 229-243. [FOC Vol. 18 eFloras
2008 ]. Missouri Botanical Garden, St. Louis, MO & Harvard University
Herbaria, Cambridge, MA. Available from:
http://www.efloras.org/florataxon.aspx?flora_id=2&taxon_id=10639.
in India– A. Sharma
