The Plant Vascular System: Evolution, Development and FunctionsF

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compelling evidence for the hypothesis that phloem-mobile 24nt sRNA can mediate in epigenetic TGS of specific genomic loci. Similar findings were reported for studies on endogenous inverted repeats that generate double-stranded RNA molecules (Dunoyer et al. 2010), as well as for transgenic plants expressing a hairpin-structured gene under the control of a viral companion-cell-specific promoter (Bai et al. 2011). In this latter case, this phloem-transmissible TGS event was shown to be inherited by subsequent progeny. Collectively, these findings support the notion that phloem-mobile sRNA can serve to regulate gene expression within developing tissues epigenetically to allow for adaptation to environmental inputs. Phloem-mobile miRNA Although generally considered to act cell-autonomously (Voinnet 2009), as mentioned above, numerous miRNAs have been detected in phloem exudates from various plant species, and the roles played by some of these have recently been established. In plants, adaptation to changing nutrient availability in the soil involves both root-to-shoot (see next section) and shoot-to-root signaling. In the case of phosphate (Pi), changes in availability within leaves leads to an upregulation in miR399 production and, subsequently, its entry into the phloem translocation stream (Lin et al. 2008; Pant et al. 2008). Delivery of miR399 into the roots results in the cleavage of the target mRNA encoding for PHO2, a ubiquitin-conjugating E2 enzyme (UBC24). This gives rise to increased uptake of Pi into these roots and restoration of Pi levels within the body of the plant. Loss of PHO2 activity probably allows for an increase in Pi transporter capacity; i.e., of influx carriers located in the outer region of the root and xylem parenchyma-located efflux carriers that function in Pi loading into the transpiration stream (Chiou and Lin 2011). Tuber induction in potato is regulated by phloem delivery of BEL5 transcripts and miR172 (Martin et al. 2009). Vascular expression of miR172 and its upregulation under tuber-inducing SD conditions suggested that this miRNA may act as a longdistance signaling component in the control of potato tuber induction. Support for this notion was provided by grafting studies involving P35S:MIR172 stocks grafted to WT potato scions. Here, tuberization occurred as early as in P35S:MIR172 potato lines. In contrast, when P35S:MIR172 scions were grafted to WT stocks, early tuber induction did not occur. Although these findings are consistent with miR172 serving as a phloem-mobile signal, it is also possible that it might act through regulation, in the CCs, of an independent mobile signal. Phloem-mobile sRNA control over host infection by parasitic plants Parasitic plants cause major losses in some regions of the world (Ejeta 2007). Recent studies have established that host Insights into Plant Vascular Biology 347 transcripts can enter into parasitic plants (Roney et al. 2007; David-Schwartz et al. 2008). The pathway for this trafficking is through the haustoria of the parasite that interconnects its vascular system to that of the host. This suggested that host invasion by parasitic plants might be controlled by phloem delivery of sRNA species designed specifically to target critical genes involved in the physiology or development of the parasitic weed (Yoder et al. 2009). Based on the observation that parasitic broomrape (Orobanche aegyptiaca) accumulates large quantities of mannitol, Aly et al. (2009) engineered transgenic tomatoes to express a hairpin construct to target the mannose 6-phosphate reductase (M6PR) that functions as a key enzyme in mannitol biosynthesis. Analysis of tissue from broomrape growing on these transgenic tomato plants indicated a significant reduction in both M6PR transcript and mannitol levels. This strategy gave rise to a level of tomato protection against this plant parasite. An alternate control approach based on targeting a parasitic developmental program involved the development of transgenic tobacco plants expressing hairpin constructs for two dodder (Cuscuta pentagona) haustoria-expressed KNOTTEDlike HOMEOBOX1 (KNOX1) genes. These constructs were driven by the CC-specific SUC2 promoter and were based on 3 ′ UTRs that did not display sequence homology to the related tobacco orthologues, STM and KNAT1–3 (Alakonya et al. 2012). Defects in haustoria development and connection to the transgenic tobacco plants were highly correlated with the presence of KNOX1 siRNA, delivered most likely through the vascular system, and down-regulation of the C. pentagona KNOX1 transcript levels. Importantly, dodder plants growing on these transgenic tobacco plants exhibited greatly reduced vigor. Collectively, these studies indicate that an effective control of plant parasitism may be achieved by targeting a pyramided combination of parasite genes involved in various aspects of growth and development. Root-to-shoot Signaling Response to abiotic stress Signals arising within the root system can provide shoots with an early warning of root conditions, such as water deficiency, nutrient availability/deficiency, and so forth (Figure 23). The xylem transports hormones, such as abscisic acid (ABA) (Bahrun et al. 2002; Jiang and Hartung 2008), ethylene and cytokinin (CK) (Takei et al. 2002; Hirose et al. 2008; Kudo et al. 2010; Ghanem et al. 2011), as well as strigolactones (SLs) (Gomez-Roldan et al. 2008; Umehara et al. 2008; Brewer et al. 2013; Ruyter-Spira et al. 2012) from roots to aboveground tissues. In this section of the review, we will address the role of these xylem-borne signaling agents.
348 Journal of Integrative Plant Biology Vol. 55 No. 4 2013 Figure 23. The plant vascular system serves as an effective inter-organ communication system. In response to a wide range of environmental and endogenous inputs, the xylem (blue lines) transmits root-to-shoot signals (blue circles), including hormones such as abscisic acid, ACC (ethylene precursor) and cytokinin, as well as strigolactones (SLs). These xylem-borne signaling agents serve to communicate the prevailing conditions within the soil. The phloem (pink lines) transports a wide array of shoot-to-root signaling molecules (pink circles), including auxin, cytokinin, proteins and RNA species, including mRNA and sRNA. These phloem-borne signaling agents complete the longdistance communication circuit that serves to integrate developmental and physiological events, occurring within shoot and root tissues, in order to optimize the plant performance under the existing growth/environmental conditions. When soils become dry, root-derived signals are transported through the xylem to leaves in order to effect a reduction in both leaf transpiration and vegetative growth. Tight control between water uptake by the root system and the xylem transpiration stream is achieved through regulation of leaf stomatal aperture. Production of ABA within roots and its transport to the leaves could contribute to preventing excess water loss, as it is has long been known that ABA is a key regulator of stomatal conductance (Mittelheuser and Van Steveninck 1969; Schachtman and Goodger 2008). The ABA content in roots is well correlated with both soil moisture and root relative water content (Davis and Zhang 1991; Thompson et al. 2007). Although large increases in ABA are detected in the xylem sap, when plants are exposed to drought conditions (Christmann et al. 2007), grafting studies have indicated that root-derived ABA is not necessary for drought-induced stomatal closure (Holbrook et al. 2002). Furthermore, recent studies have shown that leaf-derived synthesis of ABA contributes to water-stress-induced down-regulation of stomatal conductance (Holbrook et al. 2002; Thompson et al. 2007). Thus, further studies are required to evaluate the relative contribution of root-derived versus shoot-synthesized ABA in terms of the overall efficacy of stomatal control over the transpiration stream. There is some indication that ethylene-based signaling may also contribute to root-to-shoot communication under abiotic stress conditions. For example, the anaerobic environment caused by soil flooding can increase the level of aminocyclopropane carboxylic acid (ACC, the immediate precursor of ethylene) in plant roots. ACC has been detected in the xylem from both flooded and drought-stressed plants (Tudela and Primo-Millo 1992; Belimov et al. 2009). This root-derived ACC is transported to the shoot where it then gives rise to increased ethylene production which can play a role in regulating shoot growth and development under these stress conditions (Voesenek et al. 2003; Pérez-Alfocea et al. 2011). Changes in xylem sap pH have also been reported for plants exposed to drought conditions. Alkalinization of the xylem sap appears to be correlated with enhanced stomatal closure (Jia and Davies 2008; Sharp and Davies 2009). These pH changes may act synergistically with ABA and ACC to generate an effective root-to-shoot signaling system for water stress. The involvement of other known xylem-based root-toshoot signals, such as CK, etc., remains to be established in terms of contributing to water stress signaling. In any event, advancing our understanding of the mechanisms of root-toshoot signaling associated with water stress should lead the way for the development of crops with improved water use efficiencies. Xylem signals associated with nutrient stress The phenotypic plasticity that plants display in response to changes in their nutrient supply requires the operation of rootto-shoot signaling. Such signals from roots can provide shoots with an early warning of decreases in nutrient supply, while signals from shoots can ensure that the nutrient acquisition by roots is integrated to match the nutrient demand of shoots (Lough and Lucas 2006; Liu et al. 2009). CK plays an important role in plant growth and development and its involvement as a xylem-mobile signal in regulating the nutrient starvation response, such as occurs under nitrogen and phosphorus deficiency conditions, is well established (Takei et al. 2002; Hirose et al. 2008; Ghanem et al. 2011). Nitrate deprivation leads to a reduction in the level of mobile CK in the xylem sap, whereas upon resupply of nitrate to these stress
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