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Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology.

Johnston-Monje D, Raizada MN - PLoS ONE (2011)

Bottom Line: Of these traits, phosphate solubilization and production of acetoin/butanediol were the most commonly observed.An isolate from the giant Mexican landrace Mixteco, with 100% identity to Burkholderia phytofirmans, significantly promoted shoot potato biomass.Conservation and diversity in Zea-microbe relationships are discussed in the context of ecology, crop domestication, selection and migration.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Agriculture, University of Guelph, Guelph, Ontario, Canada.

ABSTRACT
Endophytes are non-pathogenic microbes living inside plants. We asked whether endophytic species were conserved in the agriculturally important plant genus Zea as it became domesticated from its wild ancestors (teosinte) to modern maize (corn) and moved from Mexico to Canada. Kernels from populations of four different teosintes and 10 different maize varieties were screened for endophytic bacteria by culturing, cloning and DNA fingerprinting using terminal restriction fragment length polymorphism (TRFLP) of 16S rDNA. Principle component analysis of TRFLP data showed that seed endophyte community composition varied in relation to plant host phylogeny. However, there was a core microbiota of endophytes that was conserved in Zea seeds across boundaries of evolution, ethnography and ecology. The majority of seed endophytes in the wild ancestor persist today in domesticated maize, though ancient selection against the hard fruitcase surrounding seeds may have altered the abundance of endophytes. Four TRFLP signals including two predicted to represent Clostridium and Paenibacillus species were conserved across all Zea genotypes, while culturing showed that Enterobacter, Methylobacteria, Pantoea and Pseudomonas species were widespread, with γ-proteobacteria being the prevalent class. Twenty-six different genera were cultured, and these were evaluated for their ability to stimulate plant growth, grow on nitrogen-free media, solubilize phosphate, sequester iron, secrete RNAse, antagonize pathogens, catabolize the precursor of ethylene, produce auxin and acetoin/butanediol. Of these traits, phosphate solubilization and production of acetoin/butanediol were the most commonly observed. An isolate from the giant Mexican landrace Mixteco, with 100% identity to Burkholderia phytofirmans, significantly promoted shoot potato biomass. GFP tagging and maize stem injection confirmed that several seed endophytes could spread systemically through the plant. One seed isolate, Enterobacter asburiae, was able to exit the root and colonize the rhizosphere. Conservation and diversity in Zea-microbe relationships are discussed in the context of ecology, crop domestication, selection and migration.

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Genetic and geographic relationships of Zea genotypes used in this study.A microsatellite based dendogram shows the known genetic relationship between genotypes, (adapted from [13]), while dotted lines show where seed originate. Group 1 maize landraces grow in semi-hot temperatures of 14–21°C under either semi-dry conditions (540 to 640 mm)(1A) or semi-wet conditions (over 650 mm)(1B). Group 2 landraces grow in hot temperatures (20 to 27°C) and semi-wet growing seasons (500 to 870 mm of precipitation). Group 3 landraces grow in very hot (24.5–27.5°C) and wet (990–1360 mm) growing seasons. Group 4 plants are found mostly at mid elevations in Western Mexico (1200–1800 m) and form very large and numerous kernels. Group 5 plants are temperate landraces. The asterisk indicates seed used were not actually grown at this location; see Table 1 for details.
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pone-0020396-g001: Genetic and geographic relationships of Zea genotypes used in this study.A microsatellite based dendogram shows the known genetic relationship between genotypes, (adapted from [13]), while dotted lines show where seed originate. Group 1 maize landraces grow in semi-hot temperatures of 14–21°C under either semi-dry conditions (540 to 640 mm)(1A) or semi-wet conditions (over 650 mm)(1B). Group 2 landraces grow in hot temperatures (20 to 27°C) and semi-wet growing seasons (500 to 870 mm of precipitation). Group 3 landraces grow in very hot (24.5–27.5°C) and wet (990–1360 mm) growing seasons. Group 4 plants are found mostly at mid elevations in Western Mexico (1200–1800 m) and form very large and numerous kernels. Group 5 plants are temperate landraces. The asterisk indicates seed used were not actually grown at this location; see Table 1 for details.

Mentions: To study the effect of Zea evolution, genetic selection and migration on seed endophytes, a diversity panel of seeds were chosen based on their evolutionary relationships and adaptations to diverse environments (Figure 1 and Table 1). A Zea species microsatellite study [10] placed Zea mays ssp. parviglumis as the primary ancestor of domesticated corn, making Parviglumis of special evolutionary interest. Another teosinte from the mountains of Mexico, Zea mays ssp. mexicana, was included as it is thought to have contributed up to 12% of maize alleles [10]. Seeds of two other more divergent teosintes were included as outgroups, Zea diploperennis, a perennial relative of maize from the mountains of Jalisco, Mexico, and Zea nicaraguensis [36], an endangered, swamp inhabiting variety from Nicaragua. As Mexican maize landraces have been organized into four main ecological groupings [13], an effort was made to include one from each (Figure 1). Two maize landraces grown in the Mexican state of Oaxaca near the proposed area of corn domestication, Mixteco and Bolita, were included as examples of ancestral maize given their position at the base of the maize lineage [10]. Mixteco (similar to the more famous Oloton landrace) was of particular interest because of its giant stature under low nutrient conditions which has previously been speculated to be attributable to the activity of beneficial endophytes [37]. The large seeds of another giant maize plant, Jala, were included in the study as Jala is prized by local peoples in the Mexican state of Jalisco for having the largest cobs in the world (up to 36 cm long); the plants are grown on rich volcanic soils [38]. The maize landraces Chapalote (a northern Mexican popcorn) and Nal-Tel (a distinctive Yucatan variety found in ancient Mayan art) were included as they are considered to be “ancient indigenous varieties” [12] that may maintain ancestral microbial associations. As maize migrated northwards with humans, varieties were selected to adapt to new environments, resulting in new landraces such as the northern Mexican Cristalino de Chihuahua [10], and ultimately the Canadian landrace Gaspe Flint, a dwarf variety that flowers under the long day temperate conditions of its northern climate and matures early before the onset of frost. Two other temperate varieties were included which might show the effects of modern breeding on maize: Pioneer 3751 is an elite hybrid cultivar that was previously used for endophyte studies [14], while B73 is an inbred yellow dent variety from the North American corn belt that was recently used in the sequencing of the maize genome [39].


Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology.

Johnston-Monje D, Raizada MN - PLoS ONE (2011)

Genetic and geographic relationships of Zea genotypes used in this study.A microsatellite based dendogram shows the known genetic relationship between genotypes, (adapted from [13]), while dotted lines show where seed originate. Group 1 maize landraces grow in semi-hot temperatures of 14–21°C under either semi-dry conditions (540 to 640 mm)(1A) or semi-wet conditions (over 650 mm)(1B). Group 2 landraces grow in hot temperatures (20 to 27°C) and semi-wet growing seasons (500 to 870 mm of precipitation). Group 3 landraces grow in very hot (24.5–27.5°C) and wet (990–1360 mm) growing seasons. Group 4 plants are found mostly at mid elevations in Western Mexico (1200–1800 m) and form very large and numerous kernels. Group 5 plants are temperate landraces. The asterisk indicates seed used were not actually grown at this location; see Table 1 for details.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3108599&req=5

pone-0020396-g001: Genetic and geographic relationships of Zea genotypes used in this study.A microsatellite based dendogram shows the known genetic relationship between genotypes, (adapted from [13]), while dotted lines show where seed originate. Group 1 maize landraces grow in semi-hot temperatures of 14–21°C under either semi-dry conditions (540 to 640 mm)(1A) or semi-wet conditions (over 650 mm)(1B). Group 2 landraces grow in hot temperatures (20 to 27°C) and semi-wet growing seasons (500 to 870 mm of precipitation). Group 3 landraces grow in very hot (24.5–27.5°C) and wet (990–1360 mm) growing seasons. Group 4 plants are found mostly at mid elevations in Western Mexico (1200–1800 m) and form very large and numerous kernels. Group 5 plants are temperate landraces. The asterisk indicates seed used were not actually grown at this location; see Table 1 for details.
Mentions: To study the effect of Zea evolution, genetic selection and migration on seed endophytes, a diversity panel of seeds were chosen based on their evolutionary relationships and adaptations to diverse environments (Figure 1 and Table 1). A Zea species microsatellite study [10] placed Zea mays ssp. parviglumis as the primary ancestor of domesticated corn, making Parviglumis of special evolutionary interest. Another teosinte from the mountains of Mexico, Zea mays ssp. mexicana, was included as it is thought to have contributed up to 12% of maize alleles [10]. Seeds of two other more divergent teosintes were included as outgroups, Zea diploperennis, a perennial relative of maize from the mountains of Jalisco, Mexico, and Zea nicaraguensis [36], an endangered, swamp inhabiting variety from Nicaragua. As Mexican maize landraces have been organized into four main ecological groupings [13], an effort was made to include one from each (Figure 1). Two maize landraces grown in the Mexican state of Oaxaca near the proposed area of corn domestication, Mixteco and Bolita, were included as examples of ancestral maize given their position at the base of the maize lineage [10]. Mixteco (similar to the more famous Oloton landrace) was of particular interest because of its giant stature under low nutrient conditions which has previously been speculated to be attributable to the activity of beneficial endophytes [37]. The large seeds of another giant maize plant, Jala, were included in the study as Jala is prized by local peoples in the Mexican state of Jalisco for having the largest cobs in the world (up to 36 cm long); the plants are grown on rich volcanic soils [38]. The maize landraces Chapalote (a northern Mexican popcorn) and Nal-Tel (a distinctive Yucatan variety found in ancient Mayan art) were included as they are considered to be “ancient indigenous varieties” [12] that may maintain ancestral microbial associations. As maize migrated northwards with humans, varieties were selected to adapt to new environments, resulting in new landraces such as the northern Mexican Cristalino de Chihuahua [10], and ultimately the Canadian landrace Gaspe Flint, a dwarf variety that flowers under the long day temperate conditions of its northern climate and matures early before the onset of frost. Two other temperate varieties were included which might show the effects of modern breeding on maize: Pioneer 3751 is an elite hybrid cultivar that was previously used for endophyte studies [14], while B73 is an inbred yellow dent variety from the North American corn belt that was recently used in the sequencing of the maize genome [39].

Bottom Line: Of these traits, phosphate solubilization and production of acetoin/butanediol were the most commonly observed.An isolate from the giant Mexican landrace Mixteco, with 100% identity to Burkholderia phytofirmans, significantly promoted shoot potato biomass.Conservation and diversity in Zea-microbe relationships are discussed in the context of ecology, crop domestication, selection and migration.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Agriculture, University of Guelph, Guelph, Ontario, Canada.

ABSTRACT
Endophytes are non-pathogenic microbes living inside plants. We asked whether endophytic species were conserved in the agriculturally important plant genus Zea as it became domesticated from its wild ancestors (teosinte) to modern maize (corn) and moved from Mexico to Canada. Kernels from populations of four different teosintes and 10 different maize varieties were screened for endophytic bacteria by culturing, cloning and DNA fingerprinting using terminal restriction fragment length polymorphism (TRFLP) of 16S rDNA. Principle component analysis of TRFLP data showed that seed endophyte community composition varied in relation to plant host phylogeny. However, there was a core microbiota of endophytes that was conserved in Zea seeds across boundaries of evolution, ethnography and ecology. The majority of seed endophytes in the wild ancestor persist today in domesticated maize, though ancient selection against the hard fruitcase surrounding seeds may have altered the abundance of endophytes. Four TRFLP signals including two predicted to represent Clostridium and Paenibacillus species were conserved across all Zea genotypes, while culturing showed that Enterobacter, Methylobacteria, Pantoea and Pseudomonas species were widespread, with γ-proteobacteria being the prevalent class. Twenty-six different genera were cultured, and these were evaluated for their ability to stimulate plant growth, grow on nitrogen-free media, solubilize phosphate, sequester iron, secrete RNAse, antagonize pathogens, catabolize the precursor of ethylene, produce auxin and acetoin/butanediol. Of these traits, phosphate solubilization and production of acetoin/butanediol were the most commonly observed. An isolate from the giant Mexican landrace Mixteco, with 100% identity to Burkholderia phytofirmans, significantly promoted shoot potato biomass. GFP tagging and maize stem injection confirmed that several seed endophytes could spread systemically through the plant. One seed isolate, Enterobacter asburiae, was able to exit the root and colonize the rhizosphere. Conservation and diversity in Zea-microbe relationships are discussed in the context of ecology, crop domestication, selection and migration.

Show MeSH
Related in: MedlinePlus