Introduction

Photosynthesis and gas exchange of leaves are affected by many stresses including drought, flooding, salinity, chilling, high temperature, soil compaction and inadequate nutrition. Many, but not all, of these stresses have symptoms in common. For example, stomatal conductance and the rate of assimilation of CO2 per unit leaf area often decrease when stress occurs. Further, it is possible that several of the stresses may exert their effects, in part, by increasing the levels of the hormone abscisic acid (ABA) in the leaf epidermis. This hormone is known to close stomata when applied to leaves.

There have been many studies of the effects of stress on gas exchange. Some have involved leaves that were fully expanded and some have been on leaves that were still expanding. Sometimes the stresses have been chronic, and sometimes they have been imposed for short periods. Sometimes the stresses have been severe, and sometimes they have been mild. Often they have been imposed more rapidly than occurs naturally.

It is thus easy to understand why interpretations have also been varied. There needs to be a more systematic approach in our studies, paying more attention to genetic differences that exist and including observations of what happens when stress is released. More teamwork may be needed to apply the range of techniques now at hand.

In this chapter we review recent developments, concentrating mostly on the effects of water stress because of its great importance, but trying where possible to identify general problems. As noted above, accumulation of ABA in leaves is common under stress, and we review its effects on gas exchange.

The study of plant responses to stress has been a central feature of plant biologists' attempts to understand how plants function in their natural and managed (agricultural/horticultural) environments. In recent years, much progress has been made in understanding how stresses affect plant performance and consequently we considered it timely to examine the ecological, physiological and biochemical responses of plants to a variety of stresses with a view to identifying common principles. In particular we were interested to see if we are now in a position to evaluate ways in which this information might be applied by plant breeders, particularly through some of the newer methods of genetic engineering, to the development of more stress-resistant crop plants.

The chapters in this book were contributed by the invited speakers at a two and a half day meeting organised by the Environmental Physiology Group of the Society for Experimental Biology and held during the Society's annual conference at Lancaster in March 1988. The meeting was also supported by the Association of Applied Biologists and the British Ecological Society. The book is divided into three parts. The first is an introductory section (Chapters 1–3) which outlines essential concepts and considers the relative importance of different stresses as limiting factors for plant production. The second section (Chapters 4–7) concerns the behaviour of plants under stress at different levels of organisation, while the third section (Chapters 8–13) considers the application of this information on stress to crop improvement both through conventional breeding and molecular biology.

The early stages of differentiation, considered in Chapter 13, are characterized by the blocking out of regions within which cells are relatively homogeneous and behave similarly. In contrast, the later stages of differentiation show highly localized specializations, often with adjacent cells differing markedly in the developmental changes they undergo. Therefore, in studying these stages of differentiation it is essential to pay close attention to the events taking place in individual cells, and this will be the first task. When this has been done, it will be necessary to return to the higher levels of organization to consider the interrelations that keep the differentiating cells as part of an organized system.

CELLULAR CHANGES DURING DIFFERENTIATION

In contrast to the body of higher animals with its large number of differentiated cell types, relatively few cell types, possibly no more than twelve, are differentiated in the body of the vascular plant. However, to describe the cellular events related to differentiation of even this small number of cell types would fill many pages. Rather than do this, attention will be concentrated on the differentiation of the tracheary elements of the xylem, the tracheids and vessel members, and the sieve elements and companion cells of the phloem. These differentiate in the primary body from procambium and in the secondary body from cambium, and because the sequence of differentiation is generally similar in both cases, it usually will not be necessary to make distinctions between them in the following description.

The continued growth of the plant body depends upon the production of new cells by mitotic activity in its meristematic regions. One might predict that this would result in a homogeneous cell population, because mitosis ordinarily leads to the formation of identical sister cells. It is obvious, however, that the plant body does not consist of such a uniform assemblage of cells. Rather, it is composed of diverse specialized cells arranged in patterns having functional significance. If this were not the case, the plant could function, at best, in only a very restricted manner. The phenomenon of differentiation, as this production of diverse cell types in definite patterns is called, has been alluded to in earlier chapters because it is almost impossible to consider growth apart from it. Now it is necessary to turn attention specifically to the phenomenon itself, one of the major topics of interest in modern developmental biology.

GENETIC CORRELATES OF DIFFERENTIATION

The diversity of differentiated cell types might suggest that genetic changes must be involved in differentiation. The preponderance of evidence, however, indicates that cellular diversity within the organism is accomplished in a framework of genetic homogeneity. The most striking evidence in support of this principle is to be found in the well-known regeneration phenomena characteristic of plants, which will be discussed fully in Chapter 17. Roots, shoots, and in many cases whole plants are often regenerated from fully differentiated cells either as a normal process or as a result of wounding or some other stimulus.

It is an interesting fact that in plant science the study of development is not equated with embryology. Although the study of embryos has made significant contributions, it is clear that the framework of developmental study in the higher plants has been provided by postembryonic stages. A very important aspect of embryonic differentiation is the establishment of shoot and root apical meristems at approximately opposite poles of the embryonic body. These meristems, whose origins differ somewhat in the various groups of vascular plants, contribute relatively little to the actual development of the embryo, but they are the centers of postembryonic development, and by their continued activity they give rise to the shoot and root systems. The shoot- and root-building activity of these meristems does not represent a mere unfolding of embryonic rudiments; rather, it is a true epigenetic formation of organs and tissues that were not present in the embryo. Thus, all aspects of development – growth and differentiation, histogenesis and organogenesis – may be investigated in relation to the activity of apical meristems, and the size and accessibility of these formative regions, in comparison to the enclosed embryo, has made them favorable sites for both descriptive and experimental studies of plant development.

In the total development of the primary plant body via its meristems, it is obvious that many processes are taking place simultaneously. There can be little doubt that these processes are interrelated and that the interaction among them holds many important keys to the understanding of the plant body, its organization, and its integrated development.

If the study of structural patterns in the shoot apices of vascular plants does not lead to an understanding of this region in functional terms, other methods of investigation must be employed to attain such an understanding. A considerable body of research has attempted to analyze more precisely the activities of the shoot tip and its component parts and has produced some new information and brought some of the more challenging unsolved problems into sharper focus. This chapter will discuss some of the significant contributions that analytical studies have made.

GROWTH OF THE SHOOT APEX

One essential function of the shoot meristem is that of producing cells. If the region is treated as a population of dividing cells, some interesting quantitative estimates of cell production can be derived. For example in Pisum sativum (garden pea) Lyndon (1968) has determined the increase in cell number in the shoot apex during a plastochron, the interval between the initiation of two successive leaves. Immediately after the initiation of a leaf primordium the apex contains 900 to 1,000 cells. While the next primordium is being formed, approximately 1,600 new cells are added so that there is nearly a threefold increase in cell number. Since the duration of a plastochron can be determined, in this case forty-eight hours, it is possible to know the average rate at which the cells are dividing. This average rate is often expressed in terms of a mean cell generation time, the average time required for all of the cells to double, that is to divide once.

The previous eight chapters have dealt with postembryonic development of the shoot. Consideration must now be given to the subsequent development of the other meristem initiated in the embryo, the root apical meristem. The organ system that develops from this meristem during the ontogeny of the plant is as extensive as the shoot system and in many cases exceeds the aerial system in size. Moreover, root systems show considerable morphological diversity and are by no means stereotyped in form or in development. Unfortunately, however, this is not generally appreciated because root systems are inaccessible to direct and sequential observation of the type that can easily be made on the shoot. Without elaborate excavation, root systems cannot be studied except in special cases, and even when exposed, they can hardly be observed ontogenetically in anything approaching normal circumstances. It is, therefore, regrettable, but not surprising, that much of our knowledge of root development is based upon laboratory-cultured seedlings of annual crop plants.

The remarkable extent of certain individual root systems has been revealed by excavation and measurement. Ecologists have long recognized that in a plant community there is usually a stratification of root systems comparable to the multiple stories of shoots. Such a layering tends to minimize competition among species for water and nutrients in the soil, and it has been shown to have an important bearing upon survival under adverse conditions.

The vascular plant, like all sexually reproducing organisms, begins its existence as a single cell, the fertilized egg or zygote. Proliferation of this cell leads to the formation of an embryo within which, at an early stage, organs and tissues begin to be formed. Early in embryogeny two distinctive regions are set apart, approximately at opposite poles, that subsequently retain the capacity for continued growth. One of these, designated the shoot apical meristem, functions to produce an expanding shoot system by the continued formation of tissues and the initiation of a succession of leaf and bud primordia. The other, the root apical meristem, similarly forms an expanding root system. Furthermore, the development of these open-ended systems is repetitive; the same kinds of tissues and organs are produced in continuing succession.

The activity of the apical meristems results in the production of a continuously elongating body, which has been called the primary body of the plant. In many cases this primary body constitutes the whole plant. In other cases, particularly in those plants with an extended lifespan, there is an additional component of development that leads to an increase in girth of the axis. This results from the activity of two additional meristems that are initiated in the postembryonic stage: the vascular cambium, which contributes additional cells to the conducting system, and the cork cambium, which produces a protective tissue replacing the original epidermis.

The fact that the activity of the vascular cambium can be traced very precisely in its mature derivatives suggests that this meristem ought to be a useful system in which to study the control of developmental phenomena. On the other hand, its relative inaccessibility to direct manipulation and to observation are obstacles to the kind of experimentation that has been so profitable in the case of the shoot apex. It is perhaps not surprising, therefore, that there has been very little experimental work dealing with the control of developmental patterns in the cambium, while at the same time such phenomena as seasonal activation have received considerable attention. There has also been a great deal of interest in the participation of the cambium in wound reactions and healing and in the establishment of tissue unions in grafts of various types, both areas of considerable applied significance. The relatively few studies that have dealt with fundamental aspects of development in the cambium, together with information that may be extracted from a number of applied investigations, give strong indications that the experimental approach could be as valuable a tool in the understanding of cambial problems as it has been in the case of the terminal meristems.

CAMBIAL INITIATION

The initiation of cambium from the primary procambial tissues, although intensively studied from the structural viewpoint, has not been investigated experimentally to the same extent.

This volume is a revised edition of a book first published, under the same title, in 1972 and now several years out of print. In recognition of the impressive body of developmental research that has been reported since the publication of the original volume, this edition has been substantially modified and modestly enlarged. The point of view of the original, however, has been retained. It is, as the title implies, structural and organismal. We have attempted to document the developmental process as the plant undergoes it, beginning with the zygote and the formation of the embryo, continuing with the development of the primary body and completing the picture with a treatment of secondary growth. We have not, therefore, undertaken to analyze phenomena like cell growth, meristematic activity, or polarity as topics in themselves, although certain phenomena, notably differentiation and the potency of differentiated cells, have been given special treatment. It may be argued that this approach could fail to reveal fundamental generalizations about development. Nevertheless, our goal was to show how the plant develops as an organism and we have attempted to adhere to it.

In the more than fifteen years that have elapsed since the original edition was published, there have been phenomenal advances in the fields of cellular and molecular biology, and these discoveries are being applied with ever-increasing intensity to the interpretation of plant development. One may reasonably ask, therefore, whether the structural and organismal approach to development has become obsolete.

The stages of leaf development discussed in the two previous chapters – the primordial stages, which culminate in a simple outgrowth at the margin of the shoot meristem, somewhat flattened on its adaxial face – give little indication of the diverse morphology of the mature leaves of various groups of vascular plants. The multipinnate frond of a fern, the needle leaves of many conifers, and the diverse simple and compound leaves of the angiosperms are remarkably similar in the period immediately following their inception. Thus, the diversity of leaf form can be interpreted best through an understanding of the later, as opposed to primordial, stages of development. On the other hand the evidence here cited indicates that in the primordial stages the leaf undergoes a determination that confers upon it a considerable degree of autonomy in its later development. Does this imply that all of the diverse morphology of leaves must be thought of as originating in a process of determination at a relatively undifferentiated stage? The answer to this question is not an easy one, and the issues involved may best be exposed by examining some of the events of later leaf development and some of the experiments that have sought to interpret them.

DEVELOPMENT OF FERN LEAVES

There is a substantial body of information about later stages of leaf development in ferns, much of it collected from species that have also been used for experimental analysis, so that descriptive and experimental data may be correlated.

In considering the apical or primary meristems of the plant body, one of the most perplexing problems is the permanently meristematic condition of these regions, which are somehow spared from the processes of maturation occurring in their derivatives. One might be tempted to relate this property to their terminal position, their three-dimensional mass, or their organization, which is distinct from that of the mature structures they produce. However, the lateral meristems, which share the capacity for continued growth but are strikingly different in every other respect, prevent an easy acquiescence to this temptation. The vascular cambium and the cork cambium, or phellogen, are lateral in position, have the form of cylindrical sheets encircling the plant axis, and are organized in close conformity with the tissues to which they give rise. They initiate only specific tissues rather than whole organs as in the case of the terminal meristems. Furthermore, it must be borne in mind that whereas every vascular plant body must have terminal meristems in order to exist at all, the lateral meristems have a supplemental role and are by no means universal (Barghoorn, 1964).

THE INITIATION OF CAMBIAL ACTIVITY

Nothing emphasizes the differences between primary and secondary meristems more effectively than a consideration of the origin of the vascular cambium. Whereas the shoot and root apical meristems are initiated among the cells of the embryo early in the development of the plant, the cambium has its origin from a partially differentiated vascular tissue, the procambium.

In order to understand developmental processes in a complex system like a plant, it is necessary to analyze parts of the system individually. Thus, in the preceding chapters the shoot apex as the initiating center of the shoot has been examined in detail, as have the initiation and development of the lateral organs to which it gives rise. The full significance of the processes that occur in these parts, however, can only be appreciated in the context of the integrated system in which they occur. It is appropriate now, therefore, to consider the development of the whole shoot system. Reflection upon the enormous diversity of shoot forms might seem to make this an impossible task, but fortunately the emergence of concepts of shoot architecture has established a framework for the analysis of varied patterns of shoot ontogeny. A relatively small number of developmental processes, occurring in various combinations, provide interpretations of widely divergent shoot forms.

This chapter will consider first the sequence of events by which the individual shoot is elaborated to its final form. It will then examine different developmental potentialities that may be expressed by shoots, often within the same shoot system. The ways in which different shoot expressions fit together into integrated shoot systems will be examined in terms of architectural concepts. Finally, these concepts will be used to interpret some of the major plant growth forms, such as trees, shrubs, and herbs.