Signalling by tips

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New molecules, including protein kinases, lipids and molecules that have neurotransmitter activities in animals have emerged as important players in tip-growing cells. Transcriptomics analysis reveals that the largest single class of genes expressed in pollen tubes encode signal transducers, reflecting the necessity to decode complex and diverse pathways that are associated with tip growth. Many of these pathways may use common intracellular second messengers, with ions and reactive oxygen species emerging as two major common denominators in many of the processes involved in tip growth. These second messengers might influence the actin cytoskeleton through known interactions with actin-binding proteins. In turn, changes in the dynamic properties of the cytoskeleton would define the basic polarity events needed to shape and modify tip-growing cells.

Introduction

Tip-growing cells undergo an extreme type of polarised growth. Their growth is based on the occurrence of elongation exclusively at the apex, which is fuelled by newly synthesised membrane delivered by vectorial exocytosis. Tip-growing cells are probably the fastest linearly growing cells in nature. Furthermore, they have been perfected by evolution as machines that sense subtle extracellular signals and environmental changes, and that develop by changing their growth axis accordingly. In plants, there are two highly differentiated types of tip-growing cells: root hairs and pollen tubes. Root hairs have to sense the soil environment and grow so as to maximise water and ion uptake; they also respond to biotic stimuli, which may result in the establishment of sophisticated symbioses. Pollen tubes, on the other hand, have to communicate their ‘self’ properties (i.e. information about species and individuality) to the external stigma cells. These cells continuously interact with the female tissues to scout and find the right path into the open ovary cavity, until they reach the micropyle’s tiny opening and deliver sperm.

The biological functions of both of these cell types imply an innate capacity to communicate with and to decode signals from their environment. It is no surprise that signalling is likely to play a central role in defining these cell types. Many groups have contributed to a significant body of new information regarding_signalling within tip-growing cells 1., 2., 3., 4., 5.. In this review, we highlight some recent developments in our understanding of signalling in apically growing plant cells. The huge amount of information compiled on the self-incompatibility system is beyond the scope of this review.

Section snippets

Re-staging a classic with new actors

Tip-growing cells have been excellent systems in which to investigate the functions of known signalling molecules and mechanisms, and in which to discover new ones [5]. The sophisticated signalling system within the pollen-tube has recently been uncovered through the study of the LePRK pollen receptor kinase signalling complex. In mature pollen, LePRK2 and LePRK1 are bound to each other in a complex, and the secreted protein LATE ANTHER TOMATO52 (LAT52) is associated with the LePRK2 [6]. In the

What the genes have to say

It is generally accepted that microsporogenesis involves the accumulation of significant levels of long-lived mRNA molecules within mature pollen; these mRNAs drive germination and early tube growth [5]. Thus, studies of the pollen transcriptome could presumably be used to define the genetic fingerprint needed for tip growth.

The importance of signalling processes in pollen relative to those in other tissues can be inferred from three recent studies of the pollen transcriptome of Arabidopsis.

Enter the ions!

Certain ions have long been known to encode information, acting as second messengers in important signalling pathways 24., 25.. Calcium ions have received particular attention 26., 27., mostly because of the so-called ‘Ca2+ signature’ but probably also because of the existence of Ca2+ switches [28]. Recent genetic evidence showed that Ca2+-ATPases are fundamental for pollen-tube growth [29]. Potassium ions also seem to play a role in this process [30] and chloride appears to be linked to the

And life met oxygen

2.5 billion years ago life met oxygen. A new aerobic environment directed the evolution of biochemical pathways towards the use of ROS. One of the ROS generation systems described in plants is dependent on NADPH-oxidase activity. Its activation requires the participation of the small cytosolic GTPases ROPs (see review by Y Gu et al., this issue). The cytoplasmic amino-terminal region of this NADPH-oxidase contains two putative EF-hand motifs, suggesting that it is regulated by Ca2+ ions 40., 41.

Dynamic skeletons: where all things come together?

ROP GTPases (see review by Y Gu et al., this issue), ionic gradients [51], lipids 17., 52., 53., and cyclic nucleotide levels 10.••, 54. all participate in signalling pathways that are known to affect the cytoskeleton. Actin-binding proteins are believed to integrate this information and to transduce it to alterations in the cytoskeleton [55]. For example, actin-depolymerising factor (ADF) and profilin act synergistically to affect actin dynamics: ADF generates more filament ends for

Conclusions

The recent advances in the field of pollen tubes and root hairs make it clear that tip-growing cells are excellent models for understanding fundamental aspects of signaling in plant cells. The analysis of the transcriptome in pollen constitutes an unprecedented basis for hypothesis-testing using the current knock-out and overexpression tools. Potentially, this may circumvent the serendipity of forward genetic screens to some extent. The simplicity and fast dynamic responses of pollen tubes and

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Sheila McCormick, Alice Cheung and Liam Dolan for comments and critical reading of the manuscript. Research in JAF’s laboratory is supported by FCT/POCTI grants (POCTI/BIA/34772/1999, POCTI/BCI/41725/2001 and POCTI/BCI/46453/2002) and fellowships for JDB (POCTI/BPD/3619/2000), ACC (POCTI/BD19874/99 and POCTI/BPD14697/2003), SSC (POCTI/BP/6453/2001) and AMP (POCTI/BP/6278/2001).

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