Non-nodulated bacterial leaf symbiosis promotes the evolutionary success of its host plants in the coffee family (Rubiaceae).

TY - JOUR

T1 - Non-nodulated bacterial leaf symbiosis promotes the evolutionary success of its host plants in the coffee family (Rubiaceae).

AU - Verstraete, Brecht

AU - Janssens, Steven

AU - Rønsted, Nina

PY - 2017/8

Y1 - 2017/8

N2 - Every plant species on Earth interacts in some way or another with microorganisms and it is well known that certain forms of symbiosis between different organisms can drive evolution. Within some clades of Rubiaceae (coffee family), a specific plant-bacteria interaction exists in which non-pathological endo- phytes are present in the leaves of their hosts. It is hypothesized that the bacterial endophytes, either alone or by interacting with the host, provide chemical protection against herbivory or pathogens by pro- ducing toxic or otherwise advantageous secondary metabolites. If the bacteria indeed have a direct ben- eficial influence on their hosts, it is reasonable to assume that the endophytes may increase the fitness of their hosts and therefore it is probable that their presence also has an influence on the long-term evolu- tion of the particular plant lineages. In this study, the possible origin in time of non-nodulated bacterial leaf symbiosis in the Vanguerieae tribe of Rubiaceae is elucidated and dissimilarities in evolutionary dynamics between species with endophytes versus species without are investigated. Bacterial leaf sym- biosis is shown to have most probably originated in the Late Miocene, a period when the savannah habi- tat is believed to have expanded on the African continent and herbivore pressure increased. The presence of bacterial leaf endophytes appears to be restricted to Old World lineages so far. Plant lineages with leaf endophytes show a significantly higher speciation rate than plant lineages without endophytes, while there is only a small difference in extinction rate. The transition rate shows that evolving towards having endophytes is twice as fast as evolving towards not having endophytes, suggesting that leaf symbiosis must be beneficial for the host plants. We conclude that the presence of bacterial leaf endophytes may also be an important driver for speciation of host plants.

AB - Every plant species on Earth interacts in some way or another with microorganisms and it is well known that certain forms of symbiosis between different organisms can drive evolution. Within some clades of Rubiaceae (coffee family), a specific plant-bacteria interaction exists in which non-pathological endo- phytes are present in the leaves of their hosts. It is hypothesized that the bacterial endophytes, either alone or by interacting with the host, provide chemical protection against herbivory or pathogens by pro- ducing toxic or otherwise advantageous secondary metabolites. If the bacteria indeed have a direct ben- eficial influence on their hosts, it is reasonable to assume that the endophytes may increase the fitness of their hosts and therefore it is probable that their presence also has an influence on the long-term evolu- tion of the particular plant lineages. In this study, the possible origin in time of non-nodulated bacterial leaf symbiosis in the Vanguerieae tribe of Rubiaceae is elucidated and dissimilarities in evolutionary dynamics between species with endophytes versus species without are investigated. Bacterial leaf sym- biosis is shown to have most probably originated in the Late Miocene, a period when the savannah habi- tat is believed to have expanded on the African continent and herbivore pressure increased. The presence of bacterial leaf endophytes appears to be restricted to Old World lineages so far. Plant lineages with leaf endophytes show a significantly higher speciation rate than plant lineages without endophytes, while there is only a small difference in extinction rate. The transition rate shows that evolving towards having endophytes is twice as fast as evolving towards not having endophytes, suggesting that leaf symbiosis must be beneficial for the host plants. We conclude that the presence of bacterial leaf endophytes may also be an important driver for speciation of host plants.

U2 - 10.1016/j.ympev.2017.05.022

DO - 10.1016/j.ympev.2017.05.022

M3 - Journal article

C2 - 28552505

SN - 1055-7903

VL - 113

SP - 161

EP - 168

JO - Molecular Phylogenetics and Evolution

JF - Molecular Phylogenetics and Evolution

ER -