9.2.3 Direct effects on cellular processes

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Some hormone systems are coupled to existing components of a cell’s physiology. This is an effective means of achieving rapid responses, often within a few minutes of alteration of hormone levels. Three cases are presented which illustrate how important direct effects can be.

(a)  Auxin and acid growth — the proton pump story

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Figure 9.10 Auxin-induced cell elongation operates through more than one mechanism. (a) Short-term growth may partly be due to acidification of the cell wall compartment due to auxin stimulation of plasma membrane H+ export (proton pump) ATPase. Here growth rates of oat coleoptile segments were measured during a 45 min incubation in solutions of different pH. (b) Specific auxin-inductable genes are expressed more abundantly in faster growing tissues, with changes in expression detectable within 10 min. These may well be related to auxin-induced growth that occurs independently of, or additively with, acid induced growth. Here tissue print autoradiagrams show distribution os SAUR (short auxin unregulated) mRNAs during gravitropic response of soybean hypocotyls. At time 0, the seedlings were moved from a vertical to horizontal position. Initially symmetrical staining is replaced by predominance of staining on the lower (faster growing) side during the bending response. The unexpanded cotyledons are just visible at the left-hand side.

(Based on Rayle and Cleland 1970 and Guilfoyle et al. 1990; (b) reproduced with permission of Plenum Publishing Corporation)

Auxin was originally viewed (1930s) as a shoot growth promoter. Unequal rates of cell elongation in cereal coleoptiles, as occurs with tropisms, was also attributed to auxin effects. We now know that auxin is active in promoting cell expansion in many other tissues: stems, roots, fruits and callus cultures. Two mechanisms seem to be involved, one in-volving rapid changes in gene expression (see Section 9.2.4(b)) and another which directly affects the cell wall. This latter may operate through what is often termed the Acid Growth Theory and relates to auxin stimulation of ‘proton pump’ ATPases located in the plasma membrane which rapidly increase H+ concentrations in the cell wall compartment (Figure 9.10a; Rayle and Cleland 1970). Low pH was originally proposed to modify some of the bonding between cell wall polymers, especially H-bonds and ionic bonds, and also to stimulate some hydrolytic enzymes. The mechanism now appears to involve cell wall proteins called expansins which are pH sensitive and interact with other cell wall polymers to modify wall mechanical properties (Cosgrove 1997). The result is a softening, or increase in plasticity, of the wall which then expands more rapidly under the driving force of turgor. The other component of wall mechanical properties is referred to as elasticity but because this is reversible deformation it does not lead to growth. Some controversy has existed on this subject since the 1970s, mainly centred on whether acid growth fully accounts for the auxin effect, and whether it is a universal phenomenon. There is little doubt that auxin stimulates proton pumping and acid-induced growth is probably at least a part of the initial growth response, but there are also acid-independent components of growth (Schopfer 1989) and other changes are needed for sustained auxin-induced growth. The discovery of auxin-stimulated genes that respond within 5 min (Section 9.2.4) suggests that direct acid-induced growth and gene expression changes may occur simultaneously.

(b)  Gibberellins and ethylene modify growth directions via control of microtubule orientation

Plant shape or form is determined by the directions in which its component organs and tissues grow. Disorganised growth in all three dimensions leads to a callus or tumour, so an organised plant clearly has spatial control of growth. Theoretically, each cell can grow in any direction, but usually the existing cell walls place some mechanical restriction on this. Cellulose microfibrils — bundles of cellulose molecules — contribute a large proportion of the strength of the primary wall, and have only limited elasticity. This means that growth along the axis of the microfibrils is restricted, but growth perpendicular to this axis can continue. Organising microfibrils into parallel arrays will therefore force pre-dominantly one-dimensional elongation growth. Microfibril orientation, in turn, is dictated by subcellular components just inside the plasma membrane called microtubules (see Section 10.1.2). Any factor that modifies the microtubule arrays can alter growth rate or direction. Indeed, gibberellin accelerates elongation rates in stems, associated with more longitudinal microtubules (Figure 10.15), and ethylene leads to radial (swelling) growth because it causes microtubules to take up more random orientations (Figure 9.11).

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Figure 9.11 Direction of cell growth is influenced by at least two hormones, gibberellin and ethylene, through effects on cellulose microfibril orientation. The microfibrils form the bulk of the strength of primary cell walls. Giberrellins lead to largely transverse orientation, which constrains growth mainly to the longitudinal direction, that is, elongation, whereas ethylene promotes a more random orientation and hence growth in all three dimensions, that is, tissue swelling. In both, the positioning of new microfibrils in the cell wall is governed by the orientation of microtubules in the cytoplasm just beneath the plasma membrane. The mechanism is described in more detail in Section 10.1.2.

(Based on Raven et al. 1992)

An intriguing exception to this is the rapid internode elongation induced by flooding of semi-aquatic species such as deepwater rice. This adaptation maintains the leaves above the hypoxic conditions within the paddy waters. Indeed, low O2 concentration is the stress signal that initiates the growth response by inducing ethylene synthesis. What is unexpected is that ethylene in this case does not lead to radial cell expansion but instead to elongation. The explanation comes from evidence that in this species ethylene increases tissue sensitivity to gibberellins, which in turn stimulate greater than normal shoot extension (Raskin and Kende 1984b). This is a neat example of inter-actions between hormones resulting in a much improved adaptation to a specific environmental problem.

(c)  ABA and stomatal guard cells

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Figure 9.12 Stomatal aperture changes are effected by movements of solutes of water in and out of guard cells, processes influenced by ABA. (a) Without ABA; (b) within minutes of additonal ABA supplied to guard cells, signal transduction pathways operating through Ca2+ and other amplification systems lead to massive pottasium ion efflux through K+-specific ion channels to the plasma membrane. Pottasium levels in the adjoining cells increase correspondingly (K+ values are in mM), Anions such as malate and chloride also move, and the net change in guard cell water potential leads to water also moving out of the guard cells by osmosis. Te reduction in cell contents lowers the turgor and cell volume, and the stomatal pore closes.

(Based on Raven et al. 1992)

We previously mentioned the role of ABA in regulating stomatal aperture. This response does not involve growth, it is rapid and reversible, and the magnitude of opening or closing is dependent on ABA concentration across a wide range. Leaf epidermis can be peeled off in a single cell layer and floated on ABA solutions, resulting in a stomatal closure response which commences within minutes. The mechanism does not seem to involve changes in gene expression, at least not initially. Instead, water and solutes are moved rapidly out of the guard cells and the change in aperture is a function of cell turgor and volume. During closure, potassium channels in the guard cell plasma membrane open, allowing potassium ions to flood out into the adjoining subsidiary cells. Anions such as malate and chloride move in the same direction to maintain electrical neutrality. This change in total solute content leads to osmotic imbalance and hence rapid water efflux from the guard cells (Figure 9.12). The resultant cell volume change is the direct cause of stomatal closure. Re-opening tends to be slower, because it takes time for the ABA level to decline and for the solutes to be moved back.

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