The Water to Solute Permeability Ratio Governs the Osmotic Volume Dynamics in Beetroot Vacuoles.
Plant cell vacuoles occupy up to 90% of the cell volume and, beyond their physiological function, are constantly subjected to water and solute exchange. The osmotic flow and vacuole volume dynamics relies on the vacuole membrane -the tonoplast- and its capacity to regulate its permeability to both water and solutes. The osmotic permeability coefficient (Pf) is the parameter that better characterizes the water transport when submitted to an osmotic gradient. Usually,Pfdeterminations are madein vitrofrom the initial rate of volume change, when a fast (almost instantaneous) osmolality change occurs. When aquaporins are present, it is accepted that initial volume changes are only due to water movements. However, in living cells osmotic changes are not necessarily abrupt but gradually imposed. Under these conditions, water flux might not be the only relevant driving force shaping the vacuole volume response. In this study, we quantitatively investigated volume dynamics of isolatedBeta vulgarisroot vacuoles under progressively applied osmotic gradients at different pH, a condition that modifies the tonoplastPf. We followed the vacuole volume changes while simultaneously determining the external osmolality time-courses and analyzing these data with mathematical modeling. Our findings indicate that vacuole volume changes, under progressively applied osmotic gradients, would not depend on the membrane elastic properties, nor on the non-osmotic volume of the vacuole, but on water and solute fluxes across the tonoplast. We found that the volume of the vacuole at the steady state is determined by the ratio of water to solute permeabilites (Pf/Ps), which in turn is ruled by pH. The dependence of the permeability ratio on pH can be interpreted in terms of the degree of aquaporin inhibition and the consequently solute transport modulation. This is relevant in many plant organs such as root, leaves, cotyledons, or stems that perform extensive rhythmic growth movements, which very likely involve considerable cell volume changes within seconds to hours.
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Instituto de Biodiversidad y Biología Experimental y Aplicada, Universidad de Buenos Aires and Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires, Argentina.
Victoria
V
Vitali
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Instituto de Biodiversidad y Biología Experimental y Aplicada, Universidad de Buenos Aires and Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires, Argentina.
Moira
M
Sutka
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Instituto de Biodiversidad y Biología Experimental y Aplicada, Universidad de Buenos Aires and Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires, Argentina.
Gabriela
G
Amodeo
System Biology Group (SysBio), Institute of Physics of Liquids and Biological Systems (IFLYSIB) CONICET, University of La PlataLa Plata, Argentina; Center for Information Services and High Performance Computing, Technische Universität DresdenDresden, Germany.
Osvaldo
O
Chara
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Instituto de Biodiversidad y Biología Experimental y Aplicada, Universidad de Buenos Aires and Consejo Nacional de Investigaciones Científicas y TécnicasBuenos Aires, Argentina; Departamento de Fisiología y Biofísica, Facultad de Medicina, Instituto de Fisiología y Biofísica (IFIBIO-Houssay), Universidad de Buenos Aires y Consejo Nacional de Investigaciones Científicas y TécnicasBuenos Aires, Argentina.
Marcelo
M
Ozu
Beta vulgaris; gradual gradients; mathematical modeling; red beet; simulation; solute flux; vacuole; water flux
Plant Physiol. 1979 Nov;64(5):837-41
16661065
J Exp Bot. 2009;60(7):2119-28
19363206
Plant Physiol. 1985 Jul;78(3):500-9
16664273
Plant Cell. 1994 May;6(5):669-683
12244253
J Membr Biol. 2002 Jun 1;187(3):175-84
12163976
FEBS Lett. 2007 May 25;581(12):2223-6
17307167
Annu Rev Plant Biol. 2011;62:273-97
21370977
Planta. 1999 Nov;210(1):80-4
10592035
Biochem J. 1979 Mar 15;178(3):539-47
454363
PLoS One. 2012;7(3):e33219
22427995
Plant Cell Environ. 2011 Jan;34(1):1-20
20946588
Science. 1992 Apr 17;256(5055):385-7
1373524
Nature. 2003 Sep 25;425(6956):393-7
14508488
J Plant Physiol. 2014 May 15;171(9):770-8
24268743
Annu Rev Plant Biol. 2012;63:183-213
22404463
Ann Bot. 2005 Sep;96(4):519-32
16024558
Plant Physiol. 1986 Aug;81(4):1147-50
16664959
J Exp Zool A Ecol Genet Physiol. 2011 Apr 1;315(4):175-202
21290610
Mol Plant. 2010 Jan;3(1):78-90
20085894
Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8547-51
8078920
Plant J. 2004 Jan;37(2):147-55
14690500
Plant Physiol. 1999 Jul;120(3):849-58
10398721
Front Plant Sci. 2014 Oct 21;5:558
25374575
Plant J. 2010 Dec;64(6):1038-47
21143683
Nature. 2001 Mar 22;410(6827):487-90
11260718
Biol Cell. 2005 Nov;97(11):837-46
15859949
Biochim Biophys Acta. 1958 Feb;27(2):229-46
13522722
FEBS Lett. 2013 Apr 2;587(7):989-93
23454640
J Math Biol. 2008 Dec;57(6):883-903
18587542
Planta. 1981 Dec;153(4):343-50
24276939
J Plant Res. 2007 Mar;120(2):193-208
17171531
Planta. 1985 May;164(2):189-200
24249560
Ann Bot. 2014 Nov;114(7):1517-33
25288632
Biophys J. 2013 Jan 8;104(1):85-95
23332061
Plant Physiol. 2001 Apr;125(4):1577-84
11299339
J Plant Res. 2007 Mar;120(2):175-89
17186120
Plant Physiol. 1976 Nov;58(5):656-62
16659738
Plant Physiol. 1979 May;63(5):828-32
16660821
Plant Physiol. 1977 Sep;60(3):339-43
16660089
Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Oct;68(4 Pt 1):041906
14682972
Plant Physiol. 1994 May;105(1):9-13
7518091
Plant Cell. 2013 Oct;25(10):4028-43
24104564
Plant Physiol. 2004 Aug;135(4):2301-17
15310831
Plant J. 2003 Jul;35(1):116-28
12834407
New Phytol. 2011 Jan;189(1):54-81
21118256
Science. 1988 Apr 8;240(4849):228
17800923
J Biol Chem. 2000 Mar 10;275(10):6777-82
10702234
Nature. 2006 Feb 9;439(7077):688-94
16340961
Front Plant Sci. 2015 Oct 27;6:873
26579140
Am J Physiol. 1998 Oct;275(4 Pt 1):C1067-80
9755060
Plant Cell. 1989 Apr;1(4):447-457
12359894
J Membr Biol. 2007 Feb;215(2-3):111-23
17568979
Front Plant Sci. 2013 Jul 02;4:231
23847636
Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):1135-40
16418285
Plant Physiol. 1997 Jul;114(3):827-834
12223745