Hybrid weakness controlled by the dosage-dependent lethal (DL) gene system in common bean (Phaseolus vulgaris) is caused by a shoot-derived inhibitory signal leading to salicylic acid-associated root death.
Certain crosses of common bean (Phaseolus vulgaris) result in temperature-dependent hybrid weakness associated with a severe root phenotype. This is controlled by the interaction of the root- and shoot-expressed semidominant alleles dosage-dependent lethal 1 (DL(1)) and DL(2), which communicate via long-distance signaling. Previously, apparent reciprocal effects on root growth and the restoration of normal root growth by exogenous sucrose led to the hypothesis that the dosage-dependent lethal (DL) system may control root-shoot carbon partitioning. Here, recombinant inbred lines were used to map the DL loci and physiological and biochemical analysis, including metabolite profiling, was used to gain new insights into the signaling interaction and the root phenotype. It is shown that the DL system does not control root-shoot carbon partitioning and that roots are unlikely to die from carbon starvation. Instead, root death likely occurs by defense-related programmed cell death, as indicated by salicylic acid accumulation. DL(2)-expressing cotyledons supply a potent inhibitory signal that is sufficient to cause such death in DL(1)-expressing roots. These data implicate the DL system in defense-related signaling and provide support for the recent hypothesis of defense-related autoimmunity as a potential isolating mechanism in plant speciation, in particular, setting a precedence for the potential roles of long-distance signaling and temperature dependence.
Hannah
Matthew A
MA
Max-Planck Institute of Molecular Plant Physiology, Am Mühlenburg 1, 14476 Golm, Germany.
Krämer
K Melanie
KM
Max-Planck Institute of Molecular Plant Physiology, Am Mühlenburg 1, 14476 Golm, Germany.
Geffroy
Valerie
V
INRA, Institut de Biotechnologie des Plantes, UMR-CNRS 8618, LPPM, bât. 630, Université Paris-Sud, 91405 Orsay, France.
Kopka
Joachim
J
Max-Planck Institute of Molecular Plant Physiology, Am Mühlenburg 1, 14476 Golm, Germany.
Blair
Matthew W
MW
Centro Internacional de Agricultura Tropical, AA 6713, Cali, Colombia.
Erban
Alexander
A
Max-Planck Institute of Molecular Plant Physiology, Am Mühlenburg 1, 14476 Golm, Germany.
Vallejos
C Eduardo
CE
Department of Horticultural Sciences, and Plant Molecular and Cellular Biology Program, 1143 Fifield Hall, University of Florida, Gainesville, FL 32611-0690, USA.
Heyer
Arnd G
AG
Biologisches Institut, Abt. Botanik, Universität Stuttgart, Pfaffenwaldring 57, D-70569 Stuttgart, Germany.
Sanders
Francis E T
FET
School of Biology.
Millner
Paul A
PA
Institute of Membrane and Systems Biology and.
Pilbeam
David J
DJ
Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK.
D050260:Carbohydrate Metabolism; D002874:Chromosome Mapping; D018548:Cotyledon / Q000502:physiology; D049810:Genetic Speciation; D006824:Hybridization, Genetic / Q000502:physiology; D027805:Phaseolus / Q000235:genetics* / Q000378:metabolism / Q000502:physiology; D018517:Plant Roots / Q000254:growth & development / Q000378:metabolism* / Q000502:physiology; D018520:Plant Shoots / Q000378:metabolism*; D020156:Salicylic Acid / Q000378:metabolism*; D015398:Signal Transduction / Q000502:physiology
D020156:Salicylic Acid