Interaction between Phosphate-Starvation, Sugar, and Cytokinin Signaling in Arabidopsis and the Roles of Cytokinin Receptors CRE1/AHK4 and AHK3

Abstract

Cytokinins control key processes during plant growth and development, and cytokinin receptors CYTOKININ RESPONSE 1/WOODEN LEG/ARABIDOPSIS HISTIDINE KINASE 4 (CRE1/WOL/AHK4), AHK2, and AHK3 have been shown to play a crucial role in this control. The involvement of cytokinins in signaling the status of several nutrients, such as sugar, nitrogen, sulfur, and phosphate (Pi), has also been highlighted, although the full physiological relevance of this role remains unclear. To gain further insights into this aspect of cytokinin action, we characterized a mutant with reduced sensitivity to cytokinin repression of a Pi starvation-responsive reporter gene and show it corresponds to AHK3. As expected, ahk3 displayed reduced responsiveness to cytokinin in callus proliferation and plant growth assays. In addition, ahk3 showed reduced cytokinin repression of several Pi starvation-responsive genes and increased sucrose sensitivity. These effects of the ahk3 mutation were especially evident in combination with the cre1 mutation, indicating partial functional redundancy between these receptors. We examined the effect of these mutations on Pi-starvation responses and found that the double mutant is not significantly affected in long-distance systemic repression of these responses. Remarkably, we found that expression of many Pi-responsive genes is stimulated by sucrose in shoots and to a lesser extent in roots, and the sugar effect in shoots of Pi-starved plants was particularly enhanced in the cre1 ahk3 double mutant. Altogether, these results indicate the existence of multidirectional cross regulation between cytokinin, sugar, and Pi-starvation signaling, thus underlining the role of cytokinin signaling in nutrient sensing and the relative importance of Pi-starvation signaling in the control of plant metabolism and development.

Vacuolar Ca2+/H+ Transport Activity Is Required for Systemic Phosphate Homeostasis Involving Shoot-to-Root Signaling in Arabidopsis

“…S2, A, C, and E), reflecting the intermediate shoot P i levels of the +/-P i plants (data not shown). In agreement with earlier observations of systemic down-regulation of several PSi genes in the 2P i root half of the split-root system (Burleigh and Harrison, 1999;Franco-Zorrilla et al, 2005;Thibaud et al, 2010), we found that the induction of SPX1, PHT1;4, and At4 in the 2P i root half was suppressed in both +/-P i wild-type and +/-P i cax1/ cax3 plants in a similar fashion (Supplemental Fig. S2, B, D, and F).…”

Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana

“…For Northern blot, 15 mg total RNA was loaded in each lane. For RNA electrophoresis, transfer to nylon membranes and hybridization was done using standard procedures 47 . The probe was amplified by PCR using primers At2g21045kF-46/ At2g21045Rp (Supplementary Data 5) and labelled with T4 polynucleotide kinase (Roche) and 50 mCi g-32 P-ATP.…”

PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 Is a Plant-Specific SEC12-Related Protein That Enables the Endoplasmic Reticulum Exit of a High-Affinity Phosphate Transporter in Arabidopsis [W]

“…Pi starvation-responsive genes are affected by cytokinins and sugars, which repress and stimulate their expression, respectively (Franco-Zorrilla et al, 2005). To determine whether the effects of these signaling molecules are altered in phf1 mutants, we examined the effects of the mutations on IPS1:GUS activity upon treatment with sugars and cytokinins ( Figure 2B).…”

“…Moreover, one member, PHT1;1 (also known as PT1), displays reduced expression in mutants of PHOSPHATE STARVATION RESPONSE1 (PHR1), a gene encoding a key transcription factor regulating Pi starvation responses (Rubio et al, 2001). In addition, like other genes of the Pi starvation regulon, expression of PHT1;1 is repressed by cytokinins and stimulated by sugars (Lejay et al, 2003;Franco-Zorrilla et al, 2005). Expression of many of these transporters is also detected in roots of plants grown under Pi-sufficient conditions and in other parts of the plant, particularly flowers and senescing leaves, suggesting that PHT1 transporters also play roles other than Pi acquisition in Pi-poor soils, such as Pi acquisition in Pi-rich soils and Pi translocation within the plant (Mudge et al, 2002).…”