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Control of vein network topology by auxin transport.

Verna C, Sawchuk MG, Linh NM, Scarpella E - BMC Biol. (2015)

Bottom Line: The transport function of tissue networks depends on topological features such as the number of networks' components and the components' connectedness; yet what controls tissue network topology is largely unknown, partly because of the difficulties in quantifying the effects of genes on tissue network topology.Finally, we find that PIN5 promotes vein formation; that all the vein-formation-promoting functions of PIN5 are redundantly inhibited by PIN6 and PIN8; and that these functions of PIN5, PIN6, and PIN8 are independent of PIN1.Our results suggest that PIN-mediated auxin transport controls the formation of veins and their connection into networks.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada. cdeagost@ualberta.ca.

ABSTRACT

Background: Tissue networks such as the vascular networks of plant and animal organs transport signals and nutrients in most multicellular organisms. The transport function of tissue networks depends on topological features such as the number of networks' components and the components' connectedness; yet what controls tissue network topology is largely unknown, partly because of the difficulties in quantifying the effects of genes on tissue network topology. We address this problem for the vein networks of plant leaves by introducing biologically motivated descriptors of vein network topology; we combine these descriptors with cellular imaging and molecular genetic analysis; and we apply this combination of approaches to leaves of Arabidopsis thaliana that lack function of, overexpress or misexpress combinations of four PIN-FORMED (PIN) genes--PIN1, PIN5, PIN6, and PIN8--which encode transporters of the plant signal auxin and are known to control vein network geometry.

Results: We find that PIN1 inhibits vein formation and connection, and that PIN6 acts redundantly to PIN1 in these processes; however, the functions of PIN6 in vein formation are nonhomologous to those of PIN1, while the functions of PIN6 in vein connection are homologous to those of PIN1. We further find that PIN8 provides functions redundant and homologous to those of PIN6 in PIN1-dependent inhibition of vein formation, but that PIN8 has no functions in PIN1/PIN6-dependent inhibition of vein connection. Finally, we find that PIN5 promotes vein formation; that all the vein-formation-promoting functions of PIN5 are redundantly inhibited by PIN6 and PIN8; and that these functions of PIN5, PIN6, and PIN8 are independent of PIN1.

Conclusions: Our results suggest that PIN-mediated auxin transport controls the formation of veins and their connection into networks.

No MeSH data available.


Expression of DR5rev::YFPnuc in pin developing leaves. a-d. Confocal laser scanning microscopy; first leaves 4 days after germination. Look-up table (ramp in c) visualizes expression levels. Top right: genotype. Bottom left: reproducibility index. Dashed white line delineates leaf primordium outline. Images in a, b, c and e were taken at identical settings and show increasingly weaker DR5rev::YFPnuc expression in pin6;8, pin1, and pin1;6. Images in a, d and f were taken by matching signal intensity to detector’s input range (~4 % saturated pixels), and show increasingly broader DR5rev::YFPnuc expression domains in pin1 and pin1;6. Bars: (a-f) 50 μm
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Fig5: Expression of DR5rev::YFPnuc in pin developing leaves. a-d. Confocal laser scanning microscopy; first leaves 4 days after germination. Look-up table (ramp in c) visualizes expression levels. Top right: genotype. Bottom left: reproducibility index. Dashed white line delineates leaf primordium outline. Images in a, b, c and e were taken at identical settings and show increasingly weaker DR5rev::YFPnuc expression in pin6;8, pin1, and pin1;6. Images in a, d and f were taken by matching signal intensity to detector’s input range (~4 % saturated pixels), and show increasingly broader DR5rev::YFPnuc expression domains in pin1 and pin1;6. Bars: (a-f) 50 μm

Mentions: As previously reported [22, 33, 38, 68], in WT the DR5 promoter was strongly active in narrow domains that coincide with sites of vein formation (Fig. 5a). Consistent with previous observations [29–33], DR5rev::YFPnuc expression was weaker in pin6;8 than in WT, but domains of DR5rev::YFPnuc expression were equally narrow in pin6;8 and WT (Fig. 5a, b). Levels of DR5rev::YFPnuc expression were lower, and domains of DR5rev::YFPnuc expression were broader, in pin1 than in WT or pin6;8 (Fig. 5a-d); and DR5rev::YFPnuc expression levels were even lower, and DR5rev::YFPnuc expression domains even broader, in pin1;6 (Fig. 5c-f).Fig. 5


Control of vein network topology by auxin transport.

Verna C, Sawchuk MG, Linh NM, Scarpella E - BMC Biol. (2015)

Expression of DR5rev::YFPnuc in pin developing leaves. a-d. Confocal laser scanning microscopy; first leaves 4 days after germination. Look-up table (ramp in c) visualizes expression levels. Top right: genotype. Bottom left: reproducibility index. Dashed white line delineates leaf primordium outline. Images in a, b, c and e were taken at identical settings and show increasingly weaker DR5rev::YFPnuc expression in pin6;8, pin1, and pin1;6. Images in a, d and f were taken by matching signal intensity to detector’s input range (~4 % saturated pixels), and show increasingly broader DR5rev::YFPnuc expression domains in pin1 and pin1;6. Bars: (a-f) 50 μm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC4641347&req=5

Fig5: Expression of DR5rev::YFPnuc in pin developing leaves. a-d. Confocal laser scanning microscopy; first leaves 4 days after germination. Look-up table (ramp in c) visualizes expression levels. Top right: genotype. Bottom left: reproducibility index. Dashed white line delineates leaf primordium outline. Images in a, b, c and e were taken at identical settings and show increasingly weaker DR5rev::YFPnuc expression in pin6;8, pin1, and pin1;6. Images in a, d and f were taken by matching signal intensity to detector’s input range (~4 % saturated pixels), and show increasingly broader DR5rev::YFPnuc expression domains in pin1 and pin1;6. Bars: (a-f) 50 μm
Mentions: As previously reported [22, 33, 38, 68], in WT the DR5 promoter was strongly active in narrow domains that coincide with sites of vein formation (Fig. 5a). Consistent with previous observations [29–33], DR5rev::YFPnuc expression was weaker in pin6;8 than in WT, but domains of DR5rev::YFPnuc expression were equally narrow in pin6;8 and WT (Fig. 5a, b). Levels of DR5rev::YFPnuc expression were lower, and domains of DR5rev::YFPnuc expression were broader, in pin1 than in WT or pin6;8 (Fig. 5a-d); and DR5rev::YFPnuc expression levels were even lower, and DR5rev::YFPnuc expression domains even broader, in pin1;6 (Fig. 5c-f).Fig. 5

Bottom Line: The transport function of tissue networks depends on topological features such as the number of networks' components and the components' connectedness; yet what controls tissue network topology is largely unknown, partly because of the difficulties in quantifying the effects of genes on tissue network topology.Finally, we find that PIN5 promotes vein formation; that all the vein-formation-promoting functions of PIN5 are redundantly inhibited by PIN6 and PIN8; and that these functions of PIN5, PIN6, and PIN8 are independent of PIN1.Our results suggest that PIN-mediated auxin transport controls the formation of veins and their connection into networks.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada. cdeagost@ualberta.ca.

ABSTRACT

Background: Tissue networks such as the vascular networks of plant and animal organs transport signals and nutrients in most multicellular organisms. The transport function of tissue networks depends on topological features such as the number of networks' components and the components' connectedness; yet what controls tissue network topology is largely unknown, partly because of the difficulties in quantifying the effects of genes on tissue network topology. We address this problem for the vein networks of plant leaves by introducing biologically motivated descriptors of vein network topology; we combine these descriptors with cellular imaging and molecular genetic analysis; and we apply this combination of approaches to leaves of Arabidopsis thaliana that lack function of, overexpress or misexpress combinations of four PIN-FORMED (PIN) genes--PIN1, PIN5, PIN6, and PIN8--which encode transporters of the plant signal auxin and are known to control vein network geometry.

Results: We find that PIN1 inhibits vein formation and connection, and that PIN6 acts redundantly to PIN1 in these processes; however, the functions of PIN6 in vein formation are nonhomologous to those of PIN1, while the functions of PIN6 in vein connection are homologous to those of PIN1. We further find that PIN8 provides functions redundant and homologous to those of PIN6 in PIN1-dependent inhibition of vein formation, but that PIN8 has no functions in PIN1/PIN6-dependent inhibition of vein connection. Finally, we find that PIN5 promotes vein formation; that all the vein-formation-promoting functions of PIN5 are redundantly inhibited by PIN6 and PIN8; and that these functions of PIN5, PIN6, and PIN8 are independent of PIN1.

Conclusions: Our results suggest that PIN-mediated auxin transport controls the formation of veins and their connection into networks.

No MeSH data available.