Journal of Agricultural Science (2005), 143, 137–150. f 2005 Cambridge University Press 137 doi:10.1017/S0021859605005083 Printed in the United Kingdom

CENTENARY REVIEW Phytomers, phyllochrons, phenology and temperate cereal development

G. S. M C MASTER 2150 Centre Ave., Bldg D, Suite 200, Fort Collins, CO, 80526, USA (Revised MS received 16 September 2004)

SUMMARY Extensive research has been conducted on temperate cereal development since the inception of the Journal of Agricultural Science, Cambridge in 1905. This review presents an overview of the orderly and predictable development of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.). It begins with the concept of building canopies by the formation, growth and senescence of phytomers (the unit comprised of the leaf, axillary bud, node and internode). Morphological naming schemes for uniquely identifying each plant part are then extended to uniquely name each phytomer unit. The role of the phyllochron (rate of leaf appearance) in synchronizing cereal development and phytomer formation is discussed, as is the use of phenology to predict the timing of the formation, growth and senescence of individual components. The complete developmental sequence of the winter wheat shoot apex correlated with growth stages is extended to spring barley. This overview discusses the abiotic factors controlling cereal development, with special attention given to key questions regarding the critical role of temperature. The review concludes with some cautious glances forward to the exciting possibilities for better understanding of mechanisms controlling the phyllochron and phe- nology being gained from advances in functional genomics and molecular biology.

INTRODUCTION Although Goethe first coined the term ‘morphology’ in the late eighteenth century, much of our scientific The grasses are a vast group, and a corr- understanding of grasses has occurred since the later espondingly vast mass of information about nineteenth century. Dissemination of knowledge was them has been accumulated by botanists. If this greatly expanded by the creation of agricultural information were brought together and corr- journals; the Journal of Agricultural Science, elated, it would form a library rather than a Cambridge was one of the earliest when first pub- volume. lished in 1905. As Agnes Arbor pointed out, by 1934 a A. Arber (1934) vast accumulation of information about grasses had been accomplished. The state of knowledge in 1934 From earliest times, humans have gathered infor- has been dwarfed by the exponential explosion of mation on plants, albeit a somewhat informal form of research in the latter half of the twentieth century, documentation until the past few centuries. Interest and one can only imagine what Agnes Arber would has been great regarding the progression of plants write today about our accumulated information. A though their life cycle and ultimately providing seeds, significant focus of the work on grasses has been on fruits, leaves, stems and tubers. In addition, knowl- the agriculturally significant temperate small-grain edge of the stage at which plants should be harvested cereals, wheat (Triticum aestivum L.) and barley for medicinal value was of vital interest. These inter- (Hordeum vulgare L.). ests increased as groups moved from hunting and An extensive conceptual framework of cereal gathering societies to agrarian cultures. Grasses have development has been devised, resulting in many played an increasingly important role in agriculture, tools for predicting cereal development with remark- and today are the dominant agricultural crops. able accuracy. The foundation of this work is that cereals develop in an orderly and predictable manner, Email: [email protected] especially when environmental conditions are not 138 G. S. M C MASTER

S15 MS S9 T1 MS S1 MS L6 L5 T2 S13 MS T11 L4 S1 T1 MS L4 T2 L3 L3

T11 L1

MS L2 MS L1

Fig. 1. Building plant canopies by the addition of phytomer units. Morphological naming schemes for vegetative tissues according to Klepper et al. (1983a) and reproductive tissue by Wilhelm & McMaster (1996). Adapted from McMaster (2002). limiting. The pattern of development remains the plastochron and phyllochron in coordinating the same for different genotypes with variation mainly phytomers is combined with the vast work on phe- occurring in the rate or duration of specific develop- nology to predict the orderly development of cereals. mental events, suggesting a strong genetic control. The review finishes with a wary glance towards the The pattern remains the same for varying environ- future and possible role of functional genomics in ments, again with variation primarily in the rate or better explaining the mechanisms controlling cereal duration of specific developmental events within a development. genotype. Some genotypes and developmental events vary more than others to specific environ- BUILDING CANOPIES mental stresses. Centennial journal issues provide opportunities Just as anatomy often views the cell as the funda- and incentives to consider the historical path leading mental building block of tissues, the phytomer can be to our current knowledge and where the path may considered the fundamental building block of plant lead in the future. Yet restraint is necessary, because canopies. Plants construct their canopies by the temperate cereal development is too vast a subject to repeated formation, expansion and senescence of a review in complete detail here, and readers are direc- basic unit, the phytomer. The phytomer concept dates ted to more detailed reviews that offer varying per- at least to Gray (1879), and the phytomer unit usually spectives (e.g. Engledow & Ramiah 1930; Evans & is defined as consisting of a leaf and the associated Grover 1940; Bonnett 1966; Milthorpe & Ivins 1966; axillary bud, node and internode (Evans & Grover Langer 1979; Kirby & Appleyard 1984; Hay & Kirby 1940). The phytomer unit originates at the shoot apex 1991; Rickman & Klepper 1995; McMaster 1997). A with the leaf initial. A shoot is constructed by the more modest goal is to present a general overview of sequential addition of phytomer units at the shoot selected key concepts of wheat and barley develop- apex. Each component of the phytomer unit can ment that emerge from these reviews. Most concepts continue to differentiate and grow, resulting in its apply to other grasses, and often all plants, and are visible appearance (Fig. 1). For instance, the leaf based on the premise that development is orderly and initial can continue to differentiate and grow, result- predictable. The fundamental purpose of this review ing in the appearance of the leaf blade from the is to describe how wheat and barley (and by inference, subtending whorl of leaves. If the axillary bud other grass) canopies are built by the formation, differentiates and grows, then a tiller may appear growth and senescence of phytomers. The role of the from the axil of the leaf in the form of a leaf blade. Cereal development and temperature 139

The associated internode may grow from cells derived the whorl of leaves and the blade length is half the from the intercalary meristem under certain condi- blade length of the penultimate leaf, the Haun stage tions leading to the separation of the nodes of each would be 2.5. phytomer on the shoot. At any stage (depending on A variety of shoot naming schemes for annual environment and genetics) of differentiation and grasses have been proposed (Katayama 1931; Jewiss growth, a phytomer component may then begin to 1972; Klepper et al. 1982, 1983a). In these naming senesce. Generally, the leaf is the primary phytomer schemes, the first culm to emerge from the seed is component that senesces, and towards the death of considered the main shoot (MS). Primary tillers are the shoot the internode tissue senesces. Each shoot is those derived from the axils of leaves on the main built in the same manner, and a field could be viewed shoot, with a designation of T#, where # refers to leaf as a population of phytomers forming, growing and number of the main shoot. For instance, T1 is the senescencing. primary tiller emerging from the axil of L1 on the MS One important consideration of this model is how (Fig. 1). Secondary tillers are those derived from pri- the axillary bud differentiates and grows. In the model mary tiller leaves and designated as T##, where the described in the previous paragraph for wheat and first # refers to the parent primary tiller number and barley, the axillary bud forms a new shoot. In some the second # is the leaf number of the parent primary annual grasses such as maize (Zea mays L.), the axil- tiller that subtends the secondary tiller. An example lary bud can either develop into another shoot or a would be the T11 tiller which emerges from the first female inflorescence (e.g. the ear). Another variation leaf of the primary tiller T1 (Fig. 1). Similar designa- of significance is whether the leaf initial continues to tions are given for tertiary (e.g. T111) and higher differentiate and grow. Once the shoot apex switches order tillers. An anomalous tiller, the coleoptile tiller, from vegetative to reproductive events at the time of is derived from the axil of the coleoptile leaf. This single double ridge, leaf initials stop further develop- primary tiller is designated as TC by some (Kirby ment. At double ridge, the ridge formed above the & Eisenberg 1966) and T0 by Klepper et al. (1982, leaf initial which develops into the spikelet could be 1983a). viewed as the ‘axillary bud’. One then could extend Once the leaf on each shoot can be uniquely named, the phytomer unit concept in the developing spike as this naming scheme is easily adapted to nodes and the leaf initial, the spikelet initial leading to the internodes, where node number (and the internode spikelet primordium, and the node and inter- above the node) is the same as the leaf number. node would ultimately be the node and internode on The leaf numbering system has been used to the rachis. develop a nomenclature for cereal root systems (Klepper et al. 1984). Each root axis is designated NAMING PLANT PARTS AND with the associated number of the node and direction PHYTOMERS of orientation in respect to the associated leaf on each shoot. What is particularly intriguing is that Recognizing that canopies are built by phytomers wheat root axes are developed in a synchronized necessitates that we be able to uniquely identify the pattern based on shoot development related to leaf phytomer units on each plant to allow precise com- appearance. munication when describing the processes. In order Nomenclature for inflorescence tissue is needed to to develop a naming scheme for phytomers, we can complete the morphological naming schemes for the build on existing morphological naming schemes for entire plant. Within grasses, Allred (1982) and Allred each part of the plant. Leaf morphological naming & Columbus (1988) delineated grass inflorescence schemes are the cornerstone of identifying each plant types and applied floral formulas. The naming con- tissue. Leaves are numbered acropetally on a shoot ventions for leaves and tillers can easily be adapted to (Jewiss 1972; Klepper et al. 1982, 1983a), with the uniquely identify the wheat and barley spike. first true leaf designated L1, the second L2, and so on Numerical scales for reporting the progression of until the flag leaf (Fig. 1). Haun (1973) formally inflorescence development were created by Klepper created a growth staging system that accounts for the et al. (1983b) and Sweet et al. (1991), in addition to total number of true leaves produced on a shoot: more traditional growth stage scales discussed below. Wilhelm & McMaster (1996) further developed this Haun stage=(nx1)+Ln=Lnx1, earlier work into a scheme for uniquely naming each [0f(Ln=L )f1] (1) nx1 spikelet and floret/kernel within a spikelet on each where n is the number of leaves that have appeared on shoot within a wheat and barley grass spike. As with the shoot, Lnx1 is the blade length of the penultimate leaves, each spikelet within the spike is numbered leaf, and Ln is the blade length of the youngest acropetally. To illustrate this, the first spikelet on the expanding leaf that is visible emerging from the main stem is denoted as MS, S1 (Fig. 1). Each floret/ sheath of the penultimate leaf. An example would be caryopsis is numbered acropetally within a spikelet as if the third leaf blade on a shoot is emerging from well, with F/C used to denote the floret or caryopsis, 140 G. S. M C MASTER respectively (e.g. MS, S4, C1 would be the basal ker- leaf primordium initiation and leaf appearance and nel in the fourth spikelet from the base of the main many terms have been applied to these processes. shoot spike). In cases such as six-rowed barley where Askenasy (1880, as cited by Erickson & Michelini multiple spikelets occur at each rachis node, the spi- 1957) first coined the term plastochron, and defined it kelets are further delineated with a lowercase letter as the interval between the formation of two success- (a, b, or c for six-rowed barley) arranged from left ive internode cells. The term was expanded later by to right when viewed with the rachis behind the Milthorpe (1956) and Esau (1965) to include the in- spikelets. terval between the initiation of successive primordia Although each leaf, node, internode, spikelet, floret, on the shoot apex. Further refinement of the concept and caryopsis can be uniquely named, the naming and generation of new terms such as auxochron schemes have not been extended to identifying the (Hancock & Barlow 1960) and phyllochron (Bunting phytomer unit directly. Rickman & Klepper (1995) & Drennan 1966) were proposed. Although confusion used the term phyllome to include the vegetative among these terms exists, general usage today uses phytomer (i.e. plastochron), extended leaf blades (i.e. the plastochron for the rate of primordium initiation phyllochron), reproductive phytomer (i.e. spikelets), and the phyllochron for the rate of leaf appearance and florets, yet this only approached a naming (Wilhelm & McMaster 1995). scheme for phytomer units. The naming schemes Depending on the species, the relationship of the for individual plant parts can easily be extended to plastochron to the phyllochron varies. For rice naming the vegetative and reproductive phytomers of (Oryza sativa L.), the plastochron rate and phyllo- wheat and barley. As with leaves that are numbered chron rate is the same (about a 1:1 ratio), while for acropetally on a shoot starting with L1, the first wheat and barley the ratio is about 2:1 where leaf phytomer associated with the first leaf is denoted with primordia are produced more quickly than they a ‘P’ and would be P1. Because it is important to appear (Baker & Gallagher 1983; Kiniry et al. 1991). know that this phytomer is associated with a leaf that The initiation of reproductive phytomers (i.e. spikelet is growing beyond the leaf initial, the use of ‘L’ is initials) tends to be about 3–4 times faster than added to the designation, giving PL1. The next phy- vegetative phytomers (i.e. leaf initials, Rickman & tomer would be PL2, etc. up to the flag leaf on the Klepper 1995; McMaster 1997). Regardless of the culm, which would be PLn, where n equals the leaf ratio, both the plastochron and phyllochron are quite number. The culm designation can be added to iden- predictable based on temperature, with other abiotic tify which shoot is being discussed (e.g. MS, PL3 for factors having secondary effects and often only after a the third phytomer on the main stem). threshold value is reached. In addition, the plasto- Once the single ridge stage is reached, the leaf in- chron and phyllochron vary among genotypes (Frank itial does not further differentiate and grow, rather & Bauer 1995) and planting dates within a year the spikelet initial does. These phytomer units can be (Baker et al. 1980; Porter et al. 1987). identified by using the spikelet naming scheme be- Unfortunately, while many data sets exist that ginning with the basal spikelet and numbering them measure the phyllochron, efforts to create equations acropetally and inserting a ‘P’ in front. For example, to accurately predict the phyllochron have not been the basal spikelet ‘phytomer’ in the spike would be very successful. Several analyses (Bindi et al. 1995; designated as PS1, and the terminal spikelet for wheat Kirby 1995; McMaster & Wilhelm 1995) have tested would be PSn. For two-rowed barley no modifica- at least nine different equations for different cultivars, tions are necessary, but six-rowed barley would add locations and environments and none was suitably the lowercase ‘a’, ‘b’, or ‘c’ discussed above to robust. The ‘best’ equations used the change of day identify the specific spikelet at each position on the length at the time of seedling emergence based largely rachis (e.g. PSb1 would be the central spikelet in the on the earlier work of Baker et al. (1980) and Porter basal spikelet position in six-rowed barley). et al. (1987). While a satisfactory correlation can be found using this relationship, it suffers from a lack of understanding of the underlying mechanisms con- THE PHYLLOCHRON AND trolling the phyllochron. To date, no satisfactory PLASTOCHRON equation has been developed. Because canopies are built by the formation, growth The phyllochron is also a useful predictor for the and senescence of phytomers, the timing of the time at which the axillary bud begins differentiation formation at the shoot apex of the phytomers and and growth leading to a new shoot. Each tiller has a subsequent growth and senescence of the phytomer window of time when the axillary bud can begin dif- components becomes of great interest. Phytomer ferentiation and growth, and once this window passes formation is dependent on the initiation of leaf the axillary bud normally does not initiate further primoridia, and therefore the rate of primoridia growth (Klepper et al. 1982). The timing of this win- initiation controls the timing of the phytomer for- dow is correlated with leaf appearance (Klepper et al. mation. Much attention has focused on the rate of 1982). The end result is that phytomers appear on Cereal development and temperature 141

Double Ridge Terminal Spikelet Anthesis (spikelet) Single Ridge

apical dome Spikelet initial leaf initial leaf primordium

PROFILE VIEW FACE VIEW

STEM EXTENSION HEADING RIPENING STAGE STAGE II STAGE 10.5 10.1 flowering STAGE (wheat) STAGE 10 9 in “boot” STAGE ligule of TILLERING last leaf 8 just last leaf visible STAGE just STAGE 7 visible 6 second STAGE node first visible 5 STAGE node leaf of stem STAGE 4 sheaths visible STAGE STAGE 3 leaf strongly 2 tillers sheaths erected 1 lengthen one tillering formed shoot begins

Fig. 2. The Feekes Growth Stage Scale (Large 1954) correlated with the approximate timing of certain shoot apex growth stages. culms and new shoots appear in plants in an orderly among growth scales, increasing efforts have been and predictable pattern based on the phyllochron and made to create a unified growth staging system both leaf number. Hay & Kirby (1991) discuss the syn- for cereals and for all crops (Lancashire et al. 1991). chrony of shoots within a plant to reach maturity at Converting among scales is sometimes difficult, and nearly the same time. guides (Bauer et al. 1983) and computer programs (Harrell et al. 1993, 1998) are available for assistance. Use of growth stage scales is so widespread and pro- PHENOLOGY vides such an important context for many plant While the population dynamics of phytomers can measurements that journals now often require some describe the pattern of construction of cereal can- indication of the growth stages during which mea- opies, it does not tell us when the switch from veg- surements were taken (Frank et al. 1997). etative to reproductive phytomers occurs or when specific phytomer components such as internodes SYNTHESIS OF THE DEVELOPMENTAL begin to elongate. The well-studied and often reviewed SEQUENCE t