6. Aquaporins and plant development
Seeds play a crucial role in the reproductive cycle and dissemination
of higher plants. Most seeds are highly desiccated organs, and extensive
and well-defined water exchanges are associated with seed maturation
and germination, the latter process including seed imbibition and
subsequent embryo growth [104]. A fine regulation of aquaporin
expression during these processes has been described in many species,
including ice plant and Brassica napus [105,106]. In particular, TIP3s of
all plant species examined show seed-specific expression and their
abundance markedly decreased during germination [107–110]. TIP3
expression may accompany the massive deposition of storage proteins,
oligosaccharides and phytins in protein storage vacuoles during late
seed development [111]. In Arabidopsis and pea, mercury derivatives
reduced the rate of seed germination and seed imbibition, respectively
[110,112], suggesting a role of aquaporins in these processes. To date,
clear genetic evidence for a role of aquaporins in seed germination has
only been provided in rice using transgenic plants with loss- and gainof-
function of OsPIP1;3. Gene expression studies further indicated that
this aquaporin may mediate the effects of NO on seed germination
[113].
A strong link between aquaporin expression, cell expansion and
plant growth has emerged in recent years. For instance, the expression
pattern of the AtTIP1;1 promoter in Arabidopsis is correlated with
cell enlargement in roots, hypocotyls, leaves and flower stems [114],
and AtTIP1;1 expression was induced by the growth-promoting phytohormone gibberellic acid (GA3) [115]. AtTIP1;1 may be involved in
the exchange of water and solutes across the tonoplast, during the formation
of the large central vacuoles of mature cells. Numerous studies
using transgenic plants also point to a positive role of aquaporins in
plant growth. For instance, over-expression of Arabidopsis AtPIP1;2 in
tobacco and of Panax ginseng PgTIP1 in Arabidopsis significantly increased
plant growth [116,117]. Whereas these results may suggest
that growth was hydraulically limited in these materials, we cannot exclude
that altered aquaporin expression resulted in stomatal deregulation
or enhanced mesophyll conductance to CO2, thereby promoting
carbon fixation and plant growth. In line with the former hypothesis,
the transgenic tobacco plants overexpressing AtPIP1;2 showed enhanced
leaf dehydration under drought stress conditions [117].
A recent work on the role of PIPs during lateral root emergence [48]
provides a more complete dissection of the role of aquaporins in plant
tissue growth. The hormone auxin, which orchestrates root growth
and development, was found to dramatically down-regulate the transcription
of nearly all of PIP and TIP genes in the Arabidopsis root, thereby
providing a fine control of aquaporin expression at the sites of lateral
root emergence. The hormone also inhibited water transport at the
cell and whole root levels. Aquaporin mutant analysis allowed demonstrating
the role of several aquaporin isoforms in facilitating root
emergence. A mathematical model was elaborated showing how aquaporin
regulation favors water influx into the root primordium, which
thereby forces its way through the surrounding layers of cells in
the main root [48]. Thus, plant roots appear to use auxin to regulate
aquaporins and therefore fine-tune water flow to speed up lateral root
emergence.
6. Aquaporins and plant developmentSeeds play a crucial role in the reproductive cycle and disseminationof higher plants. Most seeds are highly desiccated organs, and extensiveand well-defined water exchanges are associated with seed maturationand germination, the latter process including seed imbibition andsubsequent embryo growth [104]. A fine regulation of aquaporinexpression during these processes has been described in many species,including ice plant and Brassica napus [105,106]. In particular, TIP3s ofall plant species examined show seed-specific expression and theirabundance markedly decreased during germination [107–110]. TIP3expression may accompany the massive deposition of storage proteins,oligosaccharides and phytins in protein storage vacuoles during lateseed development [111]. In Arabidopsis and pea, mercury derivativesreduced the rate of seed germination and seed imbibition, respectively[110,112], suggesting a role of aquaporins in these processes. To date,clear genetic evidence for a role of aquaporins in seed germination hasonly been provided in rice using transgenic plants with loss- and gainof-function of OsPIP1;3. Gene expression studies further indicated thatthis aquaporin may mediate the effects of NO on seed germination[113].A strong link between aquaporin expression, cell expansion andplant growth has emerged in recent years. For instance, the expressionpattern of the AtTIP1;1 promoter in Arabidopsis is correlated withcell enlargement in roots, hypocotyls, leaves and flower stems [114],and AtTIP1;1 expression was induced by the growth-promoting phytohormone gibberellic acid (GA3) [115]. AtTIP1;1 may be involved inthe exchange of water and solutes across the tonoplast, during the formationof the large central vacuoles of mature cells. Numerous studiesusing transgenic plants also point to a positive role of aquaporins inplant growth. For instance, over-expression of Arabidopsis AtPIP1;2 intobacco and of Panax ginseng PgTIP1 in Arabidopsis significantly increasedplant growth [116,117]. Whereas these results may suggestthat growth was hydraulically limited in these materials, we cannot excludethat altered aquaporin expression resulted in stomatal deregulationor enhanced mesophyll conductance to CO2, thereby promotingcarbon fixation and plant growth. In line with the former hypothesis,the transgenic tobacco plants overexpressing AtPIP1;2 showed enhancedleaf dehydration under drought stress conditions [117].A recent work on the role of PIPs during lateral root emergence [48]provides a more complete dissection of the role of aquaporins in planttissue growth. The hormone auxin, which orchestrates root growthand development, was found to dramatically down-regulate the transcriptionof nearly all of PIP and TIP genes in the Arabidopsis root, therebyproviding a fine control of aquaporin expression at the sites of lateralroot emergence. The hormone also inhibited water transport at thecell and whole root levels. Aquaporin mutant analysis allowed demonstratingthe role of several aquaporin isoforms in facilitating rootemergence. A mathematical model was elaborated showing how aquaporinregulation favors water influx into the root primordium, whichthereby forces its way through the surrounding layers of cells inthe main root [48]. Thus, plant roots appear to use auxin to regulateaquaporins and therefore fine-tune water flow to speed up lateral rootemergence.
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