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AOBPreview originally published online on August 25, 2004
Annals of Botany 2004 94(4):615-621; doi:10.1093/aob/mch181
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Annals of Botany 94/4, © Annals of Botany Company 2004; all rights reserved

Amino Acids Composition of Teucrium Nutlet Proteins and their Systematic Significance

R. JUAN1, J. PASTOR1,*, F. MILLÁN2, M. ALAIZ2 and J. VIOQUE2

1 Department of Plant Biology and Ecology, University of Sevilla, 41012-Sevilla, Spain and 2 Instituto de la Grasa, Padre García Tejero 4, 41012-Sevilla, Spain

* For correspondence. E-mail jpastor{at}us.es

Received: 24 December 2003    Returned for revision: 13 May 2004    Accepted: 1 July 2004    Published electronically: 25 August 2004


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

• Background and Aims Plant species are considered as a good source of dietary proteins, although the nutritional quality of proteins depends on their amino acid composition. In this work the protein content and amino acid composition of nutlets of 21 Teucrium taxa (Lamiaceae) from Spain were analysed and their nutritional quality was compared with the minimum values established by the Food and Agriculture Organization of the United Nations (FAO). In addition, the amino acid composition was evaluated as a chemical character to clarify the taxonomic complexity in this genus.

• Methods Amino acid content of nutlets was determined after derivatization with diethyl ethoxymethylenemalonate by high-performance liquid chromatography. Previously, nutlets samples were hydrolysed and incubated in an oven at 110 °C for 24 h.

• Key Results The protein content was variable, ranging from 6·4 % in T. dunense to 43·8 % in T. algarbiense. According to the FAO values all taxa contain satisfactory amounts of leucine, threonine and valine and are deficient in lysine. The similarity analysis of Teucrium taxa using amino acid composition data did not clearly reflect the infrageneric classification of this genus.

• Conclusions Annual species, such as T. spinosum, T. aristatum and T. resupinatum showed a better balanced amino acid composition. The dendrogram partly matched with the karyological complexity of Teucrium. No correlation between amino acid composition and habitat has been observed, showing that Teucrium nutlet amino acid composition may not be strongly influenced by the environment.

Key words: Teucrium, Lamiaceae, nutlets, protein, amino acids, taxonomy, karyology


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
To find new protein sources it is necessary to continue to study the amino acid profile in wild plants (seeds, leaves, roots, etc.). This will allow the elaboration of human diets and animal feeds, as the nutritional quality of proteins depends on their amino acid composition. In general, Teucrium species usually grow in poor soils with limited water resources. So, the low nutritional requirements and bactericidal properties of Lamiaceae (Mabberley, 1978Go; Richardson, 1992Go) make Teucrium interesting from an economic point of view. Moreover, research on amino acid composition as a taxonomic character was carried out in some previous studies (Pettigrew and Watson, 1975Go; Yeoh and Watson, 1981Go; Yeoh et al., 1984Go, 1986Go, 1992Go), although none of them concerns Lamiaceae in particular.

Teucrium is a complex genus and, like many other Lamiaceae, is widely distributed in the Mediterranean region. Different taxa are shrubs, dwarf shrubs and perennial, biennial or annual herbs, and they are found in different habitats including cultivated fields, sand dunes or mountain rocks at high altitudes.

The taxonomic complexity of Teucrium is reflected in the changes that the systematics of this group have undergone since the first revision (Schreber, 1773Go). Several studies using different characteristics attempt to clarify the infrageneric delimitation of Teucrium. For example, pollen morphology (Ojeda and Díez, 1992Go; Díez et al., 1993Go), karyology (Valdés-Bermejo and Sánchez-Crespo, 1978Go), indumentum characteristics (Manzanares et al., 1983Go; Bini Maleci and Servettaz, 1991Go; Güemes et al., 1992Go; El Oualidi and Puech, 1993Go; Navarro and El Oualidi, 2000aGo) or phytochemistry (Harborne et al., 1986Go; Velasco-Negueruela and Pérez-Alonso, 1990Go) have been used.

In the present study, the amino acid composition of nutlet proteins of 21 taxa from Spain was investigated. According to Navarro and El Oualidi (2000b)Go, these taxa belong to six sections: sect. Teucrium, sect. Scorodonia, sect. Spinularia, sect. Scordium, sect. Chamaedrys and sect. Polium (see Table 1), the latter being the largest section. The taxa examined in this section are included in three subsections: subsect. Polium (T. algarbiense, T. capitatum, T. dunense, T. lusitanicum, T. reverchonii, T. similatum and T. turdetanum); subsect. Rotundifolia (T. rotundifolium); and subsect. Simplicipilosa (T. haenseleri).


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  		TABLE 1. Localities and collection dates of wild populations studied from Spain. A = annual species; P = perennial species

 
The aims of this study were to evaluate the nutritional quality of nutlet proteins according to the necessary minimum values established by the Food and Agriculture Organization of the United Nations (FAO, 1985Go, 1991Go), and to use the amino acid composition as a chemical feature to clarify the taxonomic complexity of the group.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Plant material
Most mature nutlets of Teucrium were collected from wild populations in Spain. Only a few samples were obtained from herbarium specimens. Voucher specimens of the populations studied are deposited in the Herbarium of the Department of Plant Biology and Ecology of the University of Seville (see Table 1 for details of localities and voucher information).

Amino acid analysis
Nutlet samples (10 mg) were hydrolysed with 4 ml of 6 N HCl. The solutions were sealed in tubes under nitrogen and incubated in an oven at 110 °C for 24 h. Amino acids were determined after derivatization with diethyl ethoxymethylenemalonate by high-performance liquid chromatography, according to the method of Alaíz et al. (1992)Go.

Quantification of proteins
Protein percentage was estimated from amino acid data (Hidalgo et al., 2001Go).

Statistical analysis
Data were analysed with one-way ANOVA and, where differences were significant, separations of means were performed using Tukey's test. Prior to statistical analysis, variables were checked for normality and transformed as necessary. Cluster analysis of Teucrium taxa was done with the NTSYS-pc program, employing the Bray Curtis index of dissimilarity (Bray and Curtis, 1957Go). The dissimilarity index was transformed to the index of similarity (1 – dissimilarity index) x 100.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Protein contents in Teucrium nutlets were variable, ranging from 6·4 % in T. dunense to 43·8 % in T. algarbiense (Table 2). In general, higher protein content was observed in herbs (annual or perennial herbs) than in shrubs. For example, in sect. Teucrium, herbs such as T. aristatum and T. campanulatum with 25·7 % and 30·9 %, respectively, showed a higher protein content than shrubs like T. fruticans (17·8 %) and T. pseudochamaepitys (14·0 %). Moreover, taxa in sect. Spinularia, which usually are annual herbs, generally had a protein content >20 %. The lowest protein content was observed in sect. Scorodonia. In 13 taxa the protein content, averaging 26 %, was similar to the percentage observed in many legumes (Reddy et al., 1984Go), while in the remaining taxa it was lower, being more similar to that observed in cereals (Stateus Livsmedelsverk, 1988Go).


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  		TABLE 2. Percentage of essential amino acids per 100 g protein (mean ± s.e.) in nutlets of 21 taxa of Teucrium compared to amino acid content meeting FAO recommendations. Different small letters indicate significant differences between values in the same column (Tukey's test). Columns without superscript letters indicate the absence of significant differences among species. Ala = Alanine, Asp = Aspartic acid, Cys = Cysteine, Glu = Glutamic acid, Gly = Glycine, Ser = Serine, Tyr = Tyrosine

 
The essential amino acid composition was similar in the 21 taxa studied (Table 3). The most abundant essential amino acids in decreasing order were arginine, leucine, valine, threonine, phenylalanine and isoleucine, whereas the least abundant ones were lysine, histidine, methionine and especially tryptophan. Among the essential amino acids, only isoleucine and valine showed significant differences between taxa. Teucrium similatum had the lowest value of isoleucine (2·6 %), while T. campanulatum showed the highest content of valine (6·5 %).


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  		TABLE 3. Percentage of essential amino acids/100 g protein (mean ± s.e.) in nutlets of 21 taxa of Teucrium compared to amino acid content meeting FAO recommendations. Different small letters indicate significant differences between values in the same column (Tukey's test, P < 0·05). Columns without superscript letters indicate the absence of significant differences among species. Arg = Arginine, His = Histidine, Iso = Isoleucine; Leu = Leucine, Lys = Lysine, Met = Methionine, Phe = Phenylalanine, Thr = Threonine, Try = Tryptophan, Val = Valine

 
Levels of non-essential amino acids showed more differences among taxa (Table 2). Significant differences among several taxa were observed in five of the seven non-essential amino acids. Only glutamic acid, with values close to 20 %, and cysteine, the least abundant of the non-essential amino acids, showed similar levels in all the taxa studied.

According to the FAO (1985Go, 1991Go), no taxon of Teucrium studied was deficient in leucine, threonine or valine, although all showed a deficit in lysine (like cereals; Young and Pellett, 1985Go; Galili and Larkins, 1999Go). However, differences were observed for several other amino acids. Thus, only in T. similatum did isoleucine content meet FAO (1985Go, 1991Go) recommendations, whereas T. spinosum was the only taxon with a histidine content that is satisfactory according to FAO (1985)Go recommendations. Content of sulphur amino acids (cysteine and methionine) was only similar to or higher than the standard set by the FAO (1985Go, 1991Go) in seven taxa (T. campanulatum, T. aristatum, T. scordium, T. resupinatum, T. chamaedrys and T. rotundifolium). Content of aromatic amino acids (phenylalanine and tyrosine) was generally more satisfactory, only being limiting in seven taxa (T. fruticans, T. pseudochamaepitys, T. chamaedrys, T. webbianum, T. turdetanum, T. capitatum and T. reverchonii). Tryptophan, often limiting in plant proteins, was found in the amounts recommended by FAO (1991)Go in seven taxa (T. pseudochamaepitys, T. botrys, T. chamaedrys, T. turdetanum, T. similatum, T. lusitanicum and T. capitatum).

In general, proteins from Teucrium nutlets, like most plant proteins, show an unbalanced amino acids composition (Young and Pellett, 1985Go; Baudoin and Maquet, 1999Go; Eknayake et al., 1999Go; Galili and Larkins, 1999Go), due to the fact that several amino acid do not reach levels recommended by FAO (1985Go, 1991Go). Among the studied taxa, T. spinosum showed the most balanced amino acid composition, being limiting only in lysine. Other taxa of interest from a nutritional point of view may be T. campanulatum, T. aristatum, T. scordium subsp. scordioides, T. resupinatum and T. rotundifolium which were deficient only in lysine and histidine. It seems that annual species show a better amino acid composition, since two of the four annual taxa studied (T. aristatum, T. botrys, T. resupinatum and T. spinosum) are among the species with the most balanced amino acid compositions.

A similarity analysis of the 21 Teucrium taxa studied based on the amino acid composition has been made. The software used (NTSYS) gives only one tree out of those possible (Fig. 1).



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  		FIG. 1. Clustering based on the amino acids content of 21 taxa of Teucrium according to Bray Curtis similarity index (1 – dissimilarity index x 100). C, sect. Chamaedrys; P P sect. Polium subsect. Polium; P R, sect. Polium subsect. Rotundifolia; P S, sect. Polium subsect. Simplicipilosa; Sc, sect. Scorodonia; Sm, sect. Scordium; Sp, sect. Spinularia; T, sect. Teucrium.

 
The taxa belonging to sect. Teucrium fell in three groups (A, D, E; Fig. 1) using the amino acids profile, despite being morphologically fairly well distinguished by their bluish-white flowers and the absence of glands in the corolla (Navarro, 1995Go; Navarro and El Oualidi, 2000aGo). However, these taxa have different habits: T. fruticans (group A) is a shrub up to 250 cm with entire leaves, and is the most different species; T. pseudochamaepitys (group E) is a dwarf shrub up to 50 cm with pinnatisect leaves; and T. campanulatum and T. aristatum (group D) are herbs with pinnatipartite or pinnatifid leaves. Teucrium aristatum has previously been included in T. campanulatum (Tutin and Wood, 1972Go). Among the remaining taxa (group F), annual species with resupinate corollas from sect. Scordium sensu Willkomm and Lange (1870)Go (T. resupinatum and T. spinosum) are clearly separated (group H), although lately Navarro and El Oualidi (2000b)Go included both species in sect. Spinularia Boiss. The remaining taxa of sect. Scordium sensu Willkomm (T. scordium subsp. scordioides and T. botrys), herbs with non-resupinate corollas, are grouped together in group J, with some taxa of sect. Polium (T. similatum, T. algarbiense, T. rotundifolium and T. haenseleri). Teucrium rotundifolium and T. haenseleri (subsections Rotundifolia and Simplicipilosa, respectively) were previously shown by Navarro and Rosúa (1988)Go to be morphologically closer to each other than to the other two taxa of this group (T. algarbiense and T. similatum), which belong to subsect. Polium. Group I is more heterogeneous, being formed by taxa belonging to three different sections (Scorodonia, Chamaedrys and Polium). The relationship between sections Chamaedrys and Polium has been reported by Kästner (1989)Go, who included sect. Polium in sect. Chamaedrys.

Moreover, the amino acid composition of Teucrium nutlets is congruent in many cases with the karyological complexity of the group. For example, sect. Spinularia is divided in the tree (Fig. 1) into two groups with the basic number x = 7 (T. resupinatum and T. spinosum) (Pastor, 1992Go) and x = 8 (T. botrys together with T. scordium subsp. scordioides from sect. Scordium) (van Loon and Kieft, 1980Go; Bayón, 1989Go, 1990Go). Although in this work, according to Navarro and El Oualidi (2000b)Go, T. botrys is considered to be included in sect. Spinularia, some authors have previously included this species in sect. Scordium (Ekim, 1982Go; Devesa, 1987Go; Navarro, 1995Go).

Sect. Polium, with the basic number x = 13 (Pastor, 1992Go; Navarro and El Oualidi, 2000bGo), is fragmented into four groups (see Fig. 1). The simplest, from a karyological point of view, includes T. similatum, T. algarbiense, T. rotundifolium and T. haenseleri, which are diploid or have higher ploidy but, usually, with low variation in chromosome numbers (Valdés-Bermejo and Sánchez-Crespo, 1978Go; Puech, 1978Go, 1984Go). Another group under sect. Polium is made up by T. turdetanum, T. capitatum and T. lusitanicum which are characterized by variable ploidy (diploid to hexaploid; Puech, 1972Go, 1974Go, 1978Go; Valdés-Bermejo and Sánchez-Crespo, 1978Go; Rosúa and Navarro, 1986Go). Teucrium chamaedrys, also has different ploidy levels and falls with species in this group, despite belonging to sect. Chamaedrys. With respect to the two last species belonging to sect. Polium (T. reverchonii and T. dunense), no pattern has been observed from a karyological point of view, especially in T. dunense which according to El Oualidi et al. (1996Go, 1999Go), is a complex taxon with the highest ploidy level of sect. Polium (2n = 7x = 91; Rosúa and Navarro, 1986Go).

Lastly, it has been suggested that environmental conditions may influence the amino acid profile of seed proteins (Baudoin and Maquet, 1999Go; Rhodes et al., 1999Go), but this is not seen here. Thus, even taxa with markedly different habitats like T. dunense (sand dunes) or T. scorodonia s.l. (woods) showed a similar composition.

In conclusion, the amino acid composition of nutlet proteins may provide useful information which may help clarify the taxonomic relationships of complex groups of plants like those belonging to Lamiaceae. Besides, from a nutritional point of view, the amino acid composition of the Teucrium taxa studied may increase their value, in addition to the current interest in phytotherapy and flavortherapy.


   ACKNOWLEDGEMENTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
We thank Dr T. Navarro for revising the identification of the plant material and M. Dolores García for technical assistance. This work was supported by grant AGL2001–0526.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

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