Vascular system is a node of systemic stress responses

Abstract

Activation of abscisic acid (ABA) biosynthesis is a trigger to elicit ABA-mediated biological events. We recently reported that drought-induced ABA biosynthesis occurs predominantly in vascular parenchyma cells. This work also showed that a particular set of drought inducible gene expressions initiated in the vascular system. The spatial constraint of ABA biosynthesis is supposed to be critical for directing systemic stress responses. Cellular competence to synthesize ABA and its responsiveness to developmental and environmental signals is discussed.

Plants live in a changing environment by optimizing their growth to given external cues. Among such environmental factors, regulation of water status is essential for plant life. Plant cells have machinery to adapt to the drought stress for itself as well as adaptation machinery to protect other cells by generating mobile signals to distal organs. Abscisic acid (ABA) is one of such mobile signals in which signaling and metabolic pathways are well documented. When subjected to drought stress, plants activate both ABA-dependent and ABA-independent cascades, and in turn induce the expression of large number of stress responsive genes and post-translational modifications.¹ Endo et al.,² demonstrated that vascular parenchyma cells play a key role in the activation of ABA-dependent pathway via producing drought-induced ABA.² This work also showed that the subset of drought stress-responsive genes was induced earlier in the vascular tissues than in mesophyll tissues.²

Spatial Constraint of Drought-induced ABA Biosynthesis

Plants develop the vascular system according to their growth.³ The vascular system is a multicellular network that is continuous within the plant body for transport of water and nutrients, such as sugars and amino acids.⁴ Structure of the vascular system varies among organs and plant species. In general, the vascular system is composed of xylem and phloem. Each of these tissues contains conducting cells and other cell types, such as living parenchyma cells and sclerenchyma cells that provide mechanical support. Vascular tissues and surrounding ground tissues contain a variety of specialized cell types, although the function of most of these cells remains unknown. Our study indicated that these vascular parenchyma cells act as the site to conduct drought-induced ABA synthesis.

Vascular bundle sheath cells are associated with vascular tissues function in the communication between vascular and mesophyll tissues. The vascular bundle sheath cells are reportedly shown to be involved in plant systemic stress responses to biotic and abiotic stresses. For example, vasculature plays a key role in pathogen-induced systemic acquired resistance.⁵ Locally applied excess light stress to a single leaf triggers the production of reactive oxygen species (ROS) at the leaf and the ROS production occurs systemically in distal leaves.⁶ ROS is produced in bundle sheath cells in leaves of Arabidopsis.⁷ The Arabidopsis Ascorbate peroxidase 2 (APX2) gene, which encodes a hydrogen peroxide scavenger, is expressed specifically in bundle sheath cells.⁷ The alx8 mutant that enhanced the APX2 expression in vascular tissues exhibited both drought tolerance and ABA overaccumulation.⁸ This result suggests that bundle sheath cells play a key role in both drought responses and ABA metabolism. It is interesting to investigate the function of bundle sheath cells in terms of the regulation of ABA metabolism and drought stress responses.

Our observations can be linked to previous publications concerning the drought stress responses. Why is vascular system more sensitive to drought stress than mesophyll tissues? One possible explanation is that the vascular system itself has higher sensitivity to drought stresses than mesophyll tissue. In rice leaves, it was shown that bundle sheath cells are more sensitive to drought stress than mesophyll cells in terms of alteration of chloroplast morphology and reduction in RubisCo protein levels under drought conditions.⁹ Alternatively, drought is perceived by other tissues such as roots and an unidentified mobile signal is transported through the vascular system to affect cellular status of the surrounding cells. It has been argued that root-to-shoot signal(s) are involved in drought responses of plants.^10,11 It is also worth mentioning that the cell-cell communicating signals might be different at each temporal and spatial point. Elucidating the molecular mechanisms how vascular tissues or their surrounding cells sense the external signals or hydraulic signals will be a next challenge for the plant's systems biology.

The Ability of the Cell to Synthesize ABA and to Regulate ABA Levels

The cellular ABA level is determined by its biosynthesis, inactivation and transport (Fig. 1). The induction of ABA biosynthesis ability is one of the triggers to elicit biological responses. The work reported in Endo et al.,² also indicates that the cell's ability to synthesize ABA varies among cell types. Two features of cells' abilities to synthesize ABA have to be examined when investigating its physiological role. One is the quantitative ability to synthesize ABA, here we call it competence. Melhorn et al.,¹² reported that transient expression of either AtNCED3-GFP or AAO3-GFP in guard cells of Vicia faba causes shrinking of guard cell.¹² This result indicated that guard cells of V. fava are competent to synthesize ABA. Secondly, the ability of the cell to change the cellular ABA level in response to internal and external stimuli is also important for eliciting physiological responses (especially rapid responses). Cells producing constant amount of ABA are able to trigger the physiological response indirectly only when ABA catabolism and transport activities are altered. Vascular parenchyma cells are both competent and capable to change ABA levels by regulating biosynthesis in response to dehydration. Nonetheless, it is still unclear whether the vascular parenchyma cell also controls ABA biosynthesis against other stresses or developmental cues. It is noteworthy that the expression of ABA biosynthetic enzymes such as AtABA4, AtNCEDs, AtABA2 and AAO3 was predominantly observed in vascular bundles, but also in other tissues as well.^13–16 It is likely that, not only vascular parenchyma cells, but also many other cells are competent to synthesize ABA. It is worth investigating their responsiveness to various signals in order to elucidate the physiological role of these cells. Higher resolution analyses of gene expression and hormone quantification will be necessary to reveal the type of competent cells that regulate the ABA levels to elicit the physiological responses to different stimuli.

Figure 1.

Regulation of cellular ABA levels. A change in the cellular ABA level elicits ABA-mediated plant response. The cellular ABA levels are determined by its biosynthesis, inactivation and transport. Also, reversible reaction between ABA and ABA glucose ester is also reported in the regulation of cellular ABA levels. The early steps of ABA biosynthesis occur in plastids (grey area).

Addendum to: Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E. Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol. 2008;147:1984–1993. doi: 10.1104/pp.108.116632.