Two genetically distinct pathways regulate flowering time in response to ambient temperature

BÁRBARA STRASSER; MARIANO ALVAREZ; MAXIMILIANO SANCHEZ; ANDREA CALIFANO; PABLO D. CERDÁN

Búzios, Río de Janeiro, Brasil.

Simposio; Simpósio Brasileiro de Genética Molecular de Plantas; 2009

Sociedad Brasilera de Genetica

Photoperiod and temperature are among the most important environmental variables plants monitor to trigger flowering at the appropriate season. In several overwintering species, exposure to the near freezing temperatures of wintertime promotes flowering by increasing sensitivity to extended photoperiods during springtime. In Arabidopsis, the promotion of flowering by near-freezing temperatures is due to the vernalization pathway. On the contrary, under suboptimal temperatures flowering is delayed in Arabidopsis by the thermosensory pathway, which overlaps with the autonomous pathway. In addition, the activity of photoreceptors is dependent on ambient temperature, so the thermosensory pathway may also interact with the photoperiod pathway. These pieces of evidence suggest that the flowering response to ambient temperature may result from the action of more than one pathway. Our data support the existence of two genetically different pathways that regulate the flowering response to ambient temperature, one requiring TFL1 and another one that requires ELF3. Both tfl1 and elf3 showed a reduced delay of flowering time in response to low ambient temperature, while tfl1 elf3 double mutants were essentially insensitive. The tfl1 mutation abolished the temperature response in cryptochrome mutants that are deficient in photoperiod perception, but not in phyB mutants, that have a constitutive activation of the photoperiod pathway. In turn, elf3 mutations suppressed the temperature response in phyB mutants, but not in cryptochrome mutants, further supporting the idea of two different genetic pathways. Microarray analysis revealed that tfl1 and elf3 effects are due to the activation of different sets of genes, tfl1 deregulating SOC1/AGL20, while elf3 produced low levels of CCA1 and LHY, and high levels of GI, leading to the activation of CO and FT. Overexpression of CCA1 also produced temperature insensitivity, suggesting that the insensitivity of elf3 mutants to lower temperatures could be the result of impaired CCA1 expression and circadian clock malfunction. Finally we used a concordance-GSEA (Concordance-Gene Set Enrichment Analysis) to show that both ELF3 and TFL1 have more general roles in temperature signaling. We observed a direct concordance between the changes in gene expression produced by the elf3 mutation at 23 ºC and the changes that occurred in WT plants exposed to low temperatures (16 ºC), suggesting that the elf3 mutation mimics the exposure to lower temperatures. Conversely, we found an inverse concordance between the changes in gene expression of tfl1 mutants grown at 16 ºC and the effects of low temperature in WT plants, strongly suggesting that TFL1 is required for a proper ambient temperature response. These results are more interesting after the finding that TFL1 is associated with membranes and membrane fluidity is known, in other systems, to play an important role in temperature perception.