Integration of Growth Control

Shoots and roots are interdependent for nutrients, with overall shoot growth limited by nutrients assimilated by the root, and root growth limited by fixed carbon (C) translocated from the shoot. Nitrogen (N) limitation and uptake by the root plays a key role in controlling shoot growth and, taken together, this suggests that just as in heterotrophic multicellular organisms, N (amino acid) and C (sugar) availability provide crucial cues in overall plant growth control (Lorberg and Hall 2004). In limiting conditions, nutrients are re-allocated to meristems and developing organs to sustain growth for the longest period possible. Unfortunately, the kinetics of change in nutrient concentrations, transport, and translocation have not yet been examined in whole plants with cellular or high temporal resolution. Therefore, it is presently not clear whether the growth responses observed in response to altered nutrient abundance are due to direct sensing of nutrient levels in meristematic cells, or whether these cells respond to surrogate systemic or mitogenic signals such as plant growth regulators or miRNAs. Novel tools for such measurements are currently being developed (Deuschle et al. 2006; Gu et al. 2006; Lager et al. 2006), and therefore it will be interesting to re-visit some of the experiments relating to plant-mobile nutrients to carefully re-assess plant growth responses when these nutrients are limiting.

A characteristic feature of plant adaptive growth responses is that different shoot or root apices, or leaf organs, grow at different rates. Growth of organs or meristems directly exposed to the nutrient is promoted. The spatially selective allocation of resources to meristems or organs experiencing conditions more conducive to growth than others in effect constitutes foraging behavior, in which the "winners are fed" and which may be cued by the physiology of the affected tissues. For example, if barley root systems are separated into different compartments, and the bulk of the root system is grown in nutrient-limiting conditions, then roots in a compartment that is provided with higher mineral nutrient levels grow faster and branch more, leading to a more effective exploitation of such localized resource "jackpots" (Drew and Saker 1975). Importantly, if the whole root system is uniformly exposed to optimal mineral nutrient levels, stimulated growth is not observed, indicating that the selective growth stimulation observed upon localized nutrient availability is an internally regulated process. Likewise, it was recently reported that the sun leaves, with their higher rates of photosynthesis and transpiration, import almost three times more cytokinins than shade leaves (Boonman et al. 2007). When cytokinins were applied to shaded or water-deficit leaves, these behaved like sun leaves. Taken together, these data are consistent with a model in which the rate of metabolism or physiology cues changes in plant growth regulator concentrations or flux to regulate growth activities.

All classical plant growth regulators: auxins, cytokinins, gibberellins, brassinosteroids, ethylene, and abscisic acid have been shown to be involved directly or indirectly in controlling adaptive growth responses to environmental change. Auxins are required for the initial specification of lateral shoot organs (Reinhardt et al. 2000) and lateral root initiation (Torrey 1950), but it is less clear how it is mechanistically involved in adaptive growth responses to nutrients. Cytokinins are involved in controlling sink-source relationships and the balance of shoot and root growth (Werner et al. 2001, 2003), and at least partially mediate nitrogen nutrient cues (Miyawaki et al. 2004; Rahayu et al. 2005). They may also be involved in controlling root growth rates by affecting the phase I/II transition. Gibberellins (GA) are required for auxin stimulation of root growth (Fu and Harberd 2003), for organ expansion in shoots, and for maintenance of the indeterminate state in axillary meristems, and hence are possibly involved in determining the dividing cell population size in early leaf primordia (Keller et al. 2006). Biosynthesis of GAs is enhanced in low light (Potter et al. 1999), and in high concentrations of CO2 (Teng et al. 2006), and therefore they likely play a role in stem and leaf organ growth. Brassinosteroids (BR) are required for cell expansion and cell division in leaves and roots (Nakaya et al. 2002). Their biosynthesis is stimulated by light, but since BR concentration is subjected to complex feedback mechanisms (Nomura and Bishop 2006), it is not clear whether BRs mediate light-intensity signaling. Ethylene is involved in many growth responses, particularly involving cell expansion, but is also involved in adaptive changes to leaf blade growth in low light (Vandenbussche et al. 2003). Abscisic acid (ABA), which mediates water deficiency cues, plays a negative role in leaf and root growth.

With the exception of ABA, which has been shown to stimulate expression of CDK inhibitors (KRP genes) (Wang et al. 1998), the mechanisms by which growth processes are controlled by these regulators are not yet clear. However, it is expected that growth regulators that move between different plant organs, i.e., auxin, cytokinin, ABA, as well as novel and still poorly characterized molecules (Booker et al. 2005), will play a major role in integration of growth responses at the whole plant level.

At the whole plant level, it is presently not clear whether cues that appear to promote growth (e.g., mineral nutrients and high, but not stressful, levels of light) and those that inhibit growth (e.g., water deficit or low temperature) act by the same mechanisms to modulate the activity of common targets. In other words, it is unclear whether promoting growth is relieving growth inhibition. Based on first principles, it is simpler, faster, and more economical to arrest growth, because it would suffice to interfere with an essential step, than to promote growth, which would require coordinate regulation of disparate processes. The principles underpinning plant growth regulation will become clearer once the targets of growth signaling pathways are identified and can be subjected to experimental manipulation.

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