Diversity of Rhizobium-Phaseolus Vulgaris Symbiosis: Overview and Perspectives
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Plant and Soil 252: 11–23, 2003. © 2003 FAO. Published by Kluwer Academic Publishers. Printed in the Netherlands. 11 Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives Esperanza Mart´ınez-Romero∗ Centro de Investigaci´on sobre Fijaci´on de Nitr´ogeno. UNAM. Ap. Postal 565-A. Cuernavaca, Morelos, M´exico Received 11 October 2001. Accepted in revised form 28 March 2002 Key words: biodiversity, nitrogen fixation, nodulation, Phaseolus vulgaris, Rhizobium, symbiosis Abstract Common bean (Phaseolus vulgaris) has become a cosmopolitan crop, but was originally domesticated in the Americas and has been grown in Latin America for several thousand years. Consequently an enormous diversity of bean nodulating bacteria have developed and in the centers of origin the predominant species in bean nodules is R. etli. In some areas of Latin America, inoculation, which normally promotes nodulation and nitrogen fixation is hampered by the prevalence of native strains. Many other species in addition to R. etli have been found in bean nodules in regions where bean has been introduced. Some of these species such as R. leguminosarum bv. phaseoli, R. gallicum bv. phaseoli and R. giardinii bv. phaseoli might have arisen by acquiring the phaseoli plasmid from R. etli. Others, like R. tropici, are well adapted to acid soils and high temperatures and are good inoculants for bean under these conditions. The large number of rhizobia species capable of nodulating bean supports that bean is a promiscuous host and a diversity of bean-rhizobia interactions exists. Large ranges of dinitrogen fixing capabilities have been documented among bean cultivars and commercial beans have the lowest values among legume crops. Knowledge on bean symbiosis is still incipient but could help to improve bean biological nitrogen fixation. Introduction the Andean region of South America in Northwestern Argentina, in Ecuador and in Northern Peru (Gepts, About 50 Phaseolus species are known (Maréchal et 1990; Gepts and Debouck, 1991; Tohme et al., 1995). al., 1978) but only a few, such as P. vulgaris, P. coc- Wild P. vulgaris plants exist in Mesoamerica and Ar- cineus, P. acutifolius, P. polyanthus,andP. lunatus are gentina (see Singh et al., 1991). Wild bean varieties domesticated and used as food. Amongst Phaseolus are tiny climbing plants with very small seeds. Do- the common bean (P. vulgaris) is the most extensively mestication of beans was originally dated over 7000 cultivated. In developing countries, most beans are years ago (Gepts and Debouck, 1991), but more re- grown to feed the local population, where they consti- cent analysis indicated that it began around 4000 years tute an important source of dietary protein. The main ago (Kaplan and Lynch, 1999) by selecting amongst bean producing countries are Brazil, China, India, wild P. vulgaris ecotypes for larger seeds and plants. Mexico and the USA, where yields vary between 1.65 Possibly beans were co-domesticated with maize in tonne ha−1 in the USA, to 0.7 tonne ha−1 in Brazil Mesoamerica, since both are grown in association in and 0.56 tonne ha−1 in Mexico (http://apps.fao.org). traditional agriculture in Mexico and in Peru, where Usually, the lower yields can be ascribed to inadequate the beans climb over the maize plants. Traditional ag- water supplies, diseases, pests and poor soils. Differ- ricultural practices that include intercropping, seem to ent sites of origin of Phaseolus vulgaris have been promote bean nitrogen fixation and their advantages located in Mesoamerica (middle America), and in have been recognized (Andrews and Kassam, 1976; Baudoin et al., 1997; Francis, 1986; Souza et al., ∗ FAX No: 52-73-175581. 1997; Wooley and Davis, 1991). In the 20th century, E-mail: [email protected] agronomists greatly modified traditional agricultural 12 practices by selecting for bushy beans in monocul- Diversity of rhizobia isolated from Phaseolus vul- ture in the presence of N chemical fertilizer. Most garis has been examined almost worldwide both in probably, beans with a poor capacity to fix N2 were centers of origin of bean and in introduced areas selected with the result that the percent nitrogen de- with a variety of techniques and criteria. DNA hy- rived from biological fixation is the lowest among bridization revealed the then designated R. phaseoli legumes (Isoi and Yoshida, 1991; reviewed in Hardar- as an heterogeneous group of bacteria (Crow et al., son, 1994). Graham and Halliday (1976) established 1981). Two dimensional protein patterns (Roberts et good correlations between the growth habit of beans al., 1980) and intrinsic antibiotic resistance (Beynon (climbing or bushy) and their nitrogen fixing capab- and Josey, 1980) also showed heterogeneity among ilities, with higher nitrogen-fixing activities found in these bacteria. The nifH gene hybridization patterns climbing beans. Levels of N2 fixation in early matur- and nodulation host-range allowed the distinction of ing lines are lower than those of late-maturing lines different types of strains from bean nodules in the (Wolyn et al., 1991), but although nitrogen fixation Americas (Martínez et al., 1985). These strains ex- has been improved by breeding in early maturing lines hibited a large genetic diversity in multilocus enzymes (St. Clair and Bliss, 1991) these have not been widely electrophoretic studies (Piñero et al., 1988). Repres- used. entative strains from these studies (CFN42, CIAT899 To enhance legume nodulation and nitrogen fixa- and FL27) were later designated the type or reference tion, the introduction of bacterial inoculants to agri- strains of R. tropici (Martínez-Romero et al., 1991), R. cultural fields has been a common practice for over etli bv. phaseoli (Segovia et al., 1993), and R. gallicum 100 years. Whenever the specific rhizobia are absent, bv. gallicum (Sessitsch et al., 1997b). inoculation readily enhances plant growth and yield In the three centers of bean domestication (Mex- (Singleton and Tavares, 1986; Streeter, 1994; reviews ico, Ecuador-Peru and Argentina), R. etli bv. phaseoli of Triplett and Sadowsky, 1992 and Vlassak and Van- has been found as the predominant nodule occupant derleyden, 1997). On the other hand, when native and no R. tropici has been isolated from bean nod- bacteria exist in the fields they often out-compete the ules. Likewise, R. etli bv. mimosae has not been inoculant strains that only occupy a small proportion isolated from bean nodules although it co-exists in soil of nodules as observed in some areas of Latin America with R. etli bv. phaseoli,atleastinMexico(Wang (Aguilar et al., 2001; Burgos et al., 1999; Graham, et al., 1999a). It is notable that neither R. gallicum 1981; Ramos and Boddey, 1987; review in Vlassak bv. phaseoli nor R. giardinii bv. phaseoli have been and Vanderleyden, 1997). Contrastingly, bean inocu- reported up to now from bean nodules in the cen- lation with R. tropici in Brazil has been successful ters of origin of bean in the Americas. Occasionally (Hungria et al., 2000; Mostasso et al., 2002) and bacteria other than R. etli have been encountered in Rhizobium inoculated onto beans enhanced both bean bean nodules in Mexico and they correspond to R. and maize yields when the two were grown together in gallicum (Silva et al., 2003). A large genetic diversity Peru (Pineda et al., 1994). has been documented for R. etli bv. phaseoli from the domestication centers. In Mexico, large diversity indexes were obtained with H>0.6 and 1.3 or 1.1 Diversity of rhizobia from bean nodules in nature strains per electropherotype (the latter in a limited and agricultural fields geographical area) (Caballero-Mellado and Martínez- Romero, 1999; Segovia et al., 1991; Souza et al., The study of the diversity of rhizobia, besides provid- 1994). Similarly, in Argentina no two isolates with ing valuable ecological information by defining host identical patterns of REP-PCR were observed and the preferences and predominance of strains, the genetic maximum degree of relatedness among isolates was relationships and structure of bacteria, the dynamics of about 90%. Bean nodule isolates from Ecuador and exchange of genetic material and the basis for the pro- Peru proved to be very diverse and could be divided posal of evolutionary trends, also provides the source by Box A1R-PCR into two clusters distinct from the of efficient strains to be used in inoculation trials in ag- Mexican isolates (Bernal and Graham, 2001). Fur- ricultural fields. Diversity studies which highlight new thermore, in Mexico (Souza et al., 1994) and in models such as the novel legume nodulating Burhold- Argentina (Aguilar et al., 1998) bean wild varieties eria (Moulin et al., 2001) contribute to our knowledge (small seed beans) have been found to be naturally of symbiosis. nodulated by diverse R. etli bv. phaseoli andinMexico 13 R. etli bv. phaseoli have been found as maize en- In Brazil (Hungria et al., 2000; Martínez-Romero dophytes in traditional agricultural fields where bean et al., 1991) and in Senegal and Gambia (Diouf et and maize are intercropped (Gutiérrez-Zamora and al., 2000), R. tropici and R. etli bv. phaseoli have Martínez-Romero, 2001). been found as bean nodule occupants. Additionally The genetic diversity observed in Colombian and R. giardinii and R. leguminosarum have been detec- Mexican isolates is so large that it could serve as the ted in bean nodules in Brazil (Mostasso et al., 2002). basis to propose new species (Caballero-Mellado and In Senegal and Gambia, the dominant species in bean Martínez-Romero, 1999; Eardly et al., 1995; Segovia nodules was R. etli (Diouf et al., 2000) and even in acid et al., 1991; Souza et al., 1994) but the fact that dis- soils in some areas of Brazil (Mostasso et al., 2002) the tantly related isolates share common 16S rRNA genes most prominent species was found to be R. etli but the hampered such a proposal (Eardly et al., 1995).