Evidence for unusual choice of host and haustoria by Dendrophthoe

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Abstract: We have noticed Annona squamosa, and Psidium guajava trees exhibiting heavy infection from the leafy mistletoe, Dendrophthoe falcata. The mistletoe has skipped its infection on other more common hosts viz., Mangifera indica and Achras sapota growing in the close proximities to the infected hosts. The haustoria on each of the infected hosts were distinct. On A.squamosa they occur as solitary unions while on P.guajava exhibit a network of epicortical roots. The article illustrates these observations and discusses the possible explanation to such evidences.

Main text:

Dendrophthoe falcata (L.f) Ettingsh, is a hemi-parasitic plant belonging to the mistletoe family Loranthaceae. Mistletoes, considered as an important component of biodiversity (Watson, 2001; Shaw et al., 2004), have been appraised not only due to their unique parasitic relationship with their respective hosts, their growth habits, mechanism of seed dispersal but also because of their miraculous assets of medicinal properties which includes their use as contraceptive, hepatoprotective, wound healing, anti-microbial, anti-oxidant, antinociceptive, anti-hyperlipidemic, cardioprotective (Pattanayak and Sunita, 2008; Anarthe et al, 2008a; 2008b; Gupta and Kachhawa, 2007; Gupta‌ et al‌, 2008; Tenpe et al. 2008; Shihab et al, 2006; Pattanayak and Priyashree, 2008) and even as a sympathetic medicine to take down abnormal tissue growth under cancer (Kunwar et al.2005).

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Geographically, B.Singh (1962) has reported that this leafy mistletoe is parasitic on over 300 hosts reported in India, Pakistan, Southeast Asia, and northern Australia. Until 1993, a report by Shaw III depicts a global increase of host range to 401. Within India itself among its hosts, 37 species of dicotyledons are trees, 19 are shrubs and 5 are climbers (Ghosh et al, 2002). Among these, Mangifera indica (Mango), Azadirachta indica (Neem) and Achras sapota (Sapota) are susceptible to infection by this mistletoe in India (Karunaichamy et al., 1999; Sridhar and Rao, 1978).

Among angiosperms, parasitic relationship through the formation of haustorial linkages is known to be widespread (Wilson and Calvin, 2006b). In general, haustorial connections among 72 (of the 75) ariel parasitic genera belong to either of the four types viz., epicortical roots (ERs), clasping solitary unions, wood roses, and bark strands (Calvin and Wilson, 1998). ERs may run along the host branches in either direction forming multiple points for attachment at variable intervals to the host branch while "unions" occur with single point of attachment for individual parasites to the host.

We own an in-house plant tissue culture lab at our residential area at Miyapur, Hyderabad, Andhra Pradesh, India and its backyard harbors a garden rich in flora consisting fruit trees viz., Jackfruit (Artocarpus heterophyllus), sapota, mango, guava (Psidium guajava) , sugar apple (Annona squamosa), coconut (Cocos nucifera), pomegranate (Punica granatum); ornamental flowering plants such as rose (Rosa damascene), gudhel (hibiscus rosa sinensis); medicinal plants such as curry leaves (Murraya koenigii), tulsi (Ocimum sanctum) and other wildly growing plants.

Surprisingly, we observed a lavish growth of D.falcata on sugar apple and guava trees while other more common hosts, mango and sapota exist in close vicinity of these infected host trees but were devoid of any symptoms of infection from D.falcata. Moreover, the haustoria on each of the infected hosts were markedly distinct. The one on the sugar apple branches (figure 1a-1b) were bulb like "solitary unions". Here, the infected host branch was devoid of any foliage and turned dark in colour possibly indicating nutrient depletion. The mistletoes on the guava branches (figure 1c-1f) exhibited haustorial structures of the type ER which run parallel in either direction on the guava branches establishing multiple contact points for further infection on the branch and exhibited growth of new siblings from these points indicating parasitism via colonization. Infected branches in guava though did not exhibit any visible growth retardation symptoms. Figure 1 (a-f) shows an illustrative record on our thought provoking observations as they raise numerous queries, a few outlined below:

Within the same area rich in flora for more common hosts only few were infected by D.falcata and not others.

The same mistletoe species exhibited different structures for haustorial connections in different hosts. Was it a modification for fulfilling nutritional requirements by the mistletoe on guava host if desired supply rates of mistletoe specific growth promoting metabolites or nutrients were limited? Or if it is an influence from a firm epigenetic hormonal control by the host that the parasite experiences inevitably.

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Sugar apple branch with solitary union from parasite showed growth reduction and a gradual decline in foliage while epicortical roots (ERs) with multiple points of attachment on the guava branches unexpectedly indicated no growth defects or symptoms of infection.

It has also been reported that the D.falcata exhibits floral resemblances to the host but we did not find any haustorial structures on any part of the mango tree. The haustorial solitary unions as those we found on the sugar apple tree are considered as the derivatives of the ERs and have evolved due to several hypothetical factors including increasing aridity (Hamilton and Barlow, 1963; Reid, 1987; Wilson and Calvin, 2006a; Wilson and Calvin, 2006b). Even when ERs on guava host branches had multiple points for attachment, there were no growth defects.

It is known that mistletoes have higher nutrient titer than their host (Lamont, 1983; Karunaichamy et al, 1993) and this could probably be attributed to a competitively higher water (including dissolved nutrient and growth promoting metabolite) uptake rate by the parasite at its haustorium at a point in the host branch in comparison to that in the protruding lateral ends of the branch (that extends after the haustorium). This might render key nutrients be unavailable to the host branches that could repress growth post-infection (Stewart, and Press, 1990). This may explain the growth retardation and decline in the mistletoe infected sugar apple branches.

Almost all the hemiparasitic members of the Loranthaceae tap the xylem vessels of their host to avail water and minerals but to a considerable extent produce their own supply of assimilates (Kuijt, 1969). D.falcata does not have an indigenous rooting system and is dependent on the host for water and minerals. Nutrient dynamics have shown a higher titre of N, P , K, Mg and Na in the leaves of mistletoe than the leaves of uninfected and infected hosts which may be due to differential translocation of elements within the host phloem (Prakash et al, 1967; Karunaichamy et al, 1999). Nitrogen loss is well pronounced in mistletoe infected hosts and a higher potassium levels in mistletoe is an indicative of higher transpiration rates but a lack of re-translocation system (Karunaichamy et al, 1999 and references therein). We hypothesize that the occurrence of multiple attachments might be a requirement for the parasite which (initially with a single attachment) was unable to fulfill its gains via though a considerably high uptake rate but that could not effect a threshold accumulation of specific growth promoting metabolite or mineral nutrient(s). Inline with this, the supposed metabolite might not have a key role in the host's growth metabolism. Adding to this, cumulative effect from a higher transpirational efficiency and that too from multiple attachments in ERs might work indirectly as a pump for the host facilitating more efficient translocations within the host thereby the host is able to bypass any growth abnormalities from the mistletoe infection as in the case of guava. Affect on growth of host might take a long time when the extent of mistletoe infection has exceeded the bearing capacity of the host. More extensive studies are required to establish an understanding of the fluid dynamics in such host parasite relationships.

Further we are planning to investigate if seeds from parasites on either of the hosts have the capability to infect other plants in our garden at the current instance and if so whether the occurrence of different haustorial structures from the same parasite are host specific or if other factors are responsible for such a behaviour and whether such factors if exist are dependent upon a decision by the parasite. The inevitably increasing host range and the extent of damage caused to the fruit trees indicates that it is high time to devise effective strategies towards the control of this leafy plant parasite.