Structure, function and localization
1.9 The genus Allium
Allium comprises a large growing genus with around 750 known species with the latest,
Allium akirense, having been discovered only very recently (Friesen & Fragman-sapir, 2014). The taxonomic classification is complicated, with the genus first being placed under the family Liliaceae in the older angiosperm classification. However, under the latest APGIII classification, the following hierarchy has been adopted (Khedim et al., 2013):
Clade Monocot Order: Asparagales Family: Amaryllidaceae Subfamily: Allioideae Genus: Allium
Members of the genus are broadly described as perennial plants with formation of a storage organ, mostly a bulb but also a rhizome or swollen root ( Fritsch & Friesen, 2002). A
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striking characteristic of the members of this genus is the synthesis of unique glutathione
derived secondary metabolites, collectively referred to as S-alk(en)yl-L-cysteine-sulfoxides
(ACSOs) (Randle et al., 1995). The most notable of these are trans-(+)-S-(1-propenyl)- L-
cysteine-sulfoxide (1-PRENCSO; isoalliin) and -(+)-S-(2-propenyl)- L-cysteine-sulfoxide (2-
PRENCSO; alliin) found in A. cepa (onion) and A. sativum (garlic), respectively. These are
major contributors to the characteristic aroma and pungency commonly associated with the garlic and onion respectively. Upon tissue disruption, the ACSOs react with an enzyme released called alliinase (E.C 4.4.1.4), giving rise to a range of thiosulfinates. It is the combination of these thiosulfinates which produces the characteristic flavour and aroma properties associated unique to some allium species (Kopsell & Randle, 1999). Within the genus, however, there is a large variation in accumulation of these compounds. Some species produce only a few cystiene sulfoxides (CSOs) and inactive alliinase such as the
members of subgenus Melanocrommyum, hence lacking any odour while other species
such as A. sativum, A. cepa, A. fistulosum accumulate large quantities of ACSOs ( Fritsch &
Friesen, 2002).
The genus is globally distributed with some members, such as A. schoenoprasum ,even
existing in the sub-arctic belt. The greatest amount of species variation is seen for Alliums stretching from the Mediterranean basin to central Asia. Another centre of species diversity exists in the western North America that comprises of several subgroups of the genus. This widespread occurrence with local centres of diversity indicates adaptation to diverse ecological niches (Kamenetsky & Rabinowitch, 2006).
Following the discovery of the anti-bacterial activity of allicin, a cysteine derived organosulfur compound which is also responsible for the characteristic garlic flavour (Cavallito & John, 1944), characterization of other flavour compounds became increasingly important for different species in this genus. One of the more commercially important Allium, that has been extensively studied and also accumulates the active organosulfur
compounds, the ACSOs, Allium cepa, has been the crop of choice for this study and has
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1.9.1
Onion (Allium cepa .L)
A. cepa, commonly known as onion, is one of the oldest cultivated vegetables with records
hinting at domestication of this species reaching as far back as 2700 B.C in Egypt and the 6th
century BC in Indian writings (Fritsch & Friesen, 2002). It is now cultivated as a biennial with the bulb forming in the first year leading to emergence of an umbel in the second growing
season. Asone of the principle Alliums and also an economically/horticulturally important
crop, onion owes its culinary value to a series of volatile sulfur compounds arising from the amino acid cysteine which is the first (S)-containing product of the reductive assimilation
pathway. Four major ACSOs have been found in A. cepa so far. These are trans-(+)-S-(1-
propenyl)-L-cysteine-sulfoxide (1-PRENCSO; isoalliin), (+)-S-methyl-L-cysteine-sulfoxide
(MCSO), (+)-S-proyl- L-cysteine-sulfoxide (PCSO) and cycloallin. Of these, 1-PRENCSO is the
most abundant (Kopsell & Randle, 1999). The earliest work describing a protein involved in
the enzymatic degradation of ACSOs in A. cepa was done by Kupiecki & Virtanen (1960)
and by Schwimmer et al., (1960). Following this, detailed work on S-containing flavour
compounds in A. cepa was done by Carson & Wong (1961) where, using gas liquid partition
chromatography, they identified several flavour associated S-volatiles. However, it wasn’t
until 1971 that thiopropanal-S-oxide, which is formed due to alliinase activity on 1-PRENCSO,
was identified as the lachrymatory factor in onion by Brodnitz & Pascale in 1971. Following the understanding of the importance of this class of S compounds in determining the commercially appreciated trait of flavour in the bulb, much work was done to elucidate the importance of S fertilization in the accumulation of these flavour precursors (Randle et al., 1995). The sink capacity for secondary sulfur compounds differentiates the S metabolism in
A. cepa from the model species Arabidopsis. Whereas Arabidopsis and other members of the family Brassicaceae accumulate sulfated secondary compounds, namely glucosinolates
that arise from a bifurcation in the S-assimilation pathway post APS production, A. cepa
accumulates reduced S compounds and secondary compounds arising from post cysteine synthesis (Kliebenstein et al., 2001; McCallum et al., 2011). Differences in pathway regulation of S assimilation also differs from other species. For instance, sulfur metabolism in Allium cepa and Brassica oleracea responded differently upon H2S exposure. As opposed
to B.oleracia, an increase in secondary sulfur compounds and sulfate was observed in A. cepa upon H2S exposure suggesting differences in the feedback regulation of the pathway
(Durenkamp et al., 2007). Furthermore, APS reductase activity was found to be
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shown to form a complex between ATP sulfurylase and APS reductase in vitro. However,
the existence of this complex has not yet been validated in other species (Cumming et al.,
2007). These anomalies, along with other physiological differences, such as the presence of
a storage organ in A. cepa, unlike Arabidopsis, make it an interesting candidate to study the
regulation of the S-assimilation pathway and its significance to the species.