Of pungency, pain, and naked mole rats: chili peppers revisited.

ABSTRACT

Capsaicinoids are unique to the chili pepper genus Capsicum within the plant family Solanaceae. The family is also known for species that produce powerful alkaloids such as nicotine (tobacco) and atropine (Atropa). This is the same family to which tomatoes, potatoes, and aubergines belong. Members of this family have a diversity of fruit types ranging from dry dehiscent capsules to fl eshy drupes and berries. Botanically speaking, chili peppers are berries (Knapp 2002) and capsaicinoids are synthesized mostly, if not exclusively, in the interlocular septum that separates seeds in the fruit (Stewart et al. 2007). Capsaicin and dihydrocapsaicin are the most abundant of the capsaicinoids, which are vanillin alkaloids responsible for the hot or burning sensation experienced on contact with chili peppers. This sensation is transduced by TRP (transient receptor potential) ion channels, specifi cally TRPV1 (transient receptor potential, vanilloid). TRP channels are nociceptors or noxious stimulus detectors on specialized sensory neurons. They are usually polymodal in their activation, responding to stimuli such as heat, chemicals, and protons (pH), but only at high thresholds (e.g. 42°C and pH 4) (Woolf and Ma 2007; Patapoutain et al. 2009). Consequently, nociceptors have considerable survival value since they signal the presence of extreme external and internal threats; internally they respond to the danger of tissue infl ammation and ensuing damage. They are also believed to be relatively ancient receptors, although they have not yet been found in bacteria, archaebacteria or in plants; trp-related genes have been found in fungi and the most ancient trp genes in animals have been discovered in unicellular choanofl agellates (Damann et al. 2008). The ecology of pungency in Capsicum as well as the behavioural response of organisms to capsaicin and other irritants transduced by TRP receptors provide extremely interesting insights into the evolution of plant secondary metabolites (see Borges 2001) and also into why some special higher mammals such as naked mole rats are unresponsive to these irritants. The centre of origin of pungent chili peppers is now believed to be the desert chaco of Bolivia and Peru (Walsh and Hoot 2001; Tewksbury et al. 2006). Pungency is a monophyletic derived trait, and a nonpungent species Capsicum ciliatum is regarded to be basal to all pungent taxa (Walsh and Hoot 2001). Contrary to popular conception, all wild Capsicum species are not pungent, and more importantly, nonpungent populations of pungent species also occur (Tewksbury et al. 2006). In the highlands of Bolivia, there appears to be an altitudinal gradient in pungency with the most pungent populations of at least one species, C. chacoense, occurring at the highest altitudes (Tewksbury et al. 2006). While the degree of pungency is encoded by several QTLs (Ben-Chaim et al. 2006), double recessive mutants at the Pun1 locus, which probably codes for an acyltransferase, are always non-pungent (Stewart et al. 2005). The pungent chili species are dispersed by birds since mammals are deterred by the pungency; moreover, mammalian guts destroy chili seeds and consequently mammals are not suitable seed dispersers for these species (Tewksbury and Nabhan 2001). The TRPV1 nociceptor in birds is insensitive to capsaicin although it demonstrates sensitivity to pH and heat (Jordt and Julius 2002). Non-pungent seeds of C. chacoense were found to be 12% thicker than pungent seeds, indicating a possible trade-off between the production of capsaicin and seed coat lignin in the phenylpropanoid pathway (Tewksbury et al. 2008b); however, since capsaicin had a constipative effect on birds, affecting the retention of seeds in their guts, pungent seeds with thinner seed coats were retained longer and suffered more damage in the gut. Yet, the longer that seeds were retained in the guts of dispersal agents, the farther they may move from their parent plants. This movement away from parental sites is usually considered an advantage since it affords escape.