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Effector Diversification Contributes to Xanthomonas oryzae pv. oryzae Phenotypic Adaptation in a Semi-Isolated Environment

View Article: PubMed Central - PubMed

ABSTRACT

Understanding the processes that shaped contemporary pathogen populations in agricultural landscapes is quite important to define appropriate management strategies and to support crop improvement efforts. Here, we took advantage of an historical record to examine the adaptation pathway of the rice pathogen Xanthomonas oryzae pv. oryzae (Xoo) in a semi-isolated environment represented in the Philippine archipelago. By comparing genomes of key Xoo groups we showed that modern populations derived from three Asian lineages. We also showed that diversification of virulence factors occurred within each lineage, most likely driven by host adaptation, and it was essential to shape contemporary pathogen races. This finding is particularly important because it expands our understanding of pathogen adaptation to modern agriculture.

No MeSH data available.


Frequency of Xanthomonas oryzae pv. oryzae (Xoo) races in the Philippine archipelago during a 40-year collection period (1972 to 2012).Color blocks represent the different races described in the Xoo database. The number of Xoo entries that were collected in the following periods are: 1972–1976 = 75, 1977–1981 = 34, 1982–1986 = 59, 1986–1992 = 133, 1993–1997 = 861, 1998–2002 = 861, 2003–2007 = 237, and 2007–2012 = 104.
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f1: Frequency of Xanthomonas oryzae pv. oryzae (Xoo) races in the Philippine archipelago during a 40-year collection period (1972 to 2012).Color blocks represent the different races described in the Xoo database. The number of Xoo entries that were collected in the following periods are: 1972–1976 = 75, 1977–1981 = 34, 1982–1986 = 59, 1986–1992 = 133, 1993–1997 = 861, 1998–2002 = 861, 2003–2007 = 237, and 2007–2012 = 104.

Mentions: The emergence of novel pathogen populations is a common phenomenon in the agricultural landscape that can be associated with drastic events of selection37. To investigate the historical dynamics of Xoo races, we mined a well-characterized dataset spanning 40 years of bacterial blight collections in the Philippines. The database recorded 10 races and 5 derived subgroups collected between 1972 and 2012 (Supplementary Table S1). We plotted the time distribution of all major races to describe two major population shifts that coincide with the emergence of novel groups during the 70s and 90s (Fig. 1). In the first case, Race 2 replaced the prevalent type Race 1 in response to change in rice cultivars across the Philippines. The event was documented by Mew et al.2 who attributed the emergence of Race 2, a Xa4-compatible population, to the wide cultivation of modern varieties carrying this gene during the early 70s. The second case describes the emergence of Race 9b as the most prevalent group after the 1992 epidemics (Fig. 1). In contrast to what appears to drive the expansion of Race 2, it is highly unlikely that single resistance gene deployment could explain the expansion of Race 9b across the entire archipelago. Besides the apparent fitness of Race 9b, we speculate that changes in cropping patterns, fertilizer use, or environmental events may have also contributed to its expansion. To our knowledge, two major events may have played a role: 1) the eruption of the Pinatubo volcano in 1991 which might caused changes in the environmental conditions of the whole archipelago38 and 2) the sudden decrease in harvested area of the dominant variety IR64, which was estimated to be 40% in 1992 but less than 1% by 201219. This mining exercise helps us to contextualize our understanding of Xoo populations and to select representatives of key races for comparative genomics.


Effector Diversification Contributes to Xanthomonas oryzae pv. oryzae Phenotypic Adaptation in a Semi-Isolated Environment
Frequency of Xanthomonas oryzae pv. oryzae (Xoo) races in the Philippine archipelago during a 40-year collection period (1972 to 2012).Color blocks represent the different races described in the Xoo database. The number of Xoo entries that were collected in the following periods are: 1972–1976 = 75, 1977–1981 = 34, 1982–1986 = 59, 1986–1992 = 133, 1993–1997 = 861, 1998–2002 = 861, 2003–2007 = 237, and 2007–2012 = 104.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5035989&req=5

f1: Frequency of Xanthomonas oryzae pv. oryzae (Xoo) races in the Philippine archipelago during a 40-year collection period (1972 to 2012).Color blocks represent the different races described in the Xoo database. The number of Xoo entries that were collected in the following periods are: 1972–1976 = 75, 1977–1981 = 34, 1982–1986 = 59, 1986–1992 = 133, 1993–1997 = 861, 1998–2002 = 861, 2003–2007 = 237, and 2007–2012 = 104.
Mentions: The emergence of novel pathogen populations is a common phenomenon in the agricultural landscape that can be associated with drastic events of selection37. To investigate the historical dynamics of Xoo races, we mined a well-characterized dataset spanning 40 years of bacterial blight collections in the Philippines. The database recorded 10 races and 5 derived subgroups collected between 1972 and 2012 (Supplementary Table S1). We plotted the time distribution of all major races to describe two major population shifts that coincide with the emergence of novel groups during the 70s and 90s (Fig. 1). In the first case, Race 2 replaced the prevalent type Race 1 in response to change in rice cultivars across the Philippines. The event was documented by Mew et al.2 who attributed the emergence of Race 2, a Xa4-compatible population, to the wide cultivation of modern varieties carrying this gene during the early 70s. The second case describes the emergence of Race 9b as the most prevalent group after the 1992 epidemics (Fig. 1). In contrast to what appears to drive the expansion of Race 2, it is highly unlikely that single resistance gene deployment could explain the expansion of Race 9b across the entire archipelago. Besides the apparent fitness of Race 9b, we speculate that changes in cropping patterns, fertilizer use, or environmental events may have also contributed to its expansion. To our knowledge, two major events may have played a role: 1) the eruption of the Pinatubo volcano in 1991 which might caused changes in the environmental conditions of the whole archipelago38 and 2) the sudden decrease in harvested area of the dominant variety IR64, which was estimated to be 40% in 1992 but less than 1% by 201219. This mining exercise helps us to contextualize our understanding of Xoo populations and to select representatives of key races for comparative genomics.

View Article: PubMed Central - PubMed

ABSTRACT

Understanding the processes that shaped contemporary pathogen populations in agricultural landscapes is quite important to define appropriate management strategies and to support crop improvement efforts. Here, we took advantage of an historical record to examine the adaptation pathway of the rice pathogen Xanthomonas oryzae pv. oryzae (Xoo) in a semi-isolated environment represented in the Philippine archipelago. By comparing genomes of key Xoo groups we showed that modern populations derived from three Asian lineages. We also showed that diversification of virulence factors occurred within each lineage, most likely driven by host adaptation, and it was essential to shape contemporary pathogen races. This finding is particularly important because it expands our understanding of pathogen adaptation to modern agriculture.

No MeSH data available.