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CROP ECOLOGY, PRODUCTION & MANAGEMENT

A Uniform, Objective, and Adaptive System for Expressing Rice Development

^a University of Arkansas, Rice Research and Extension Center, P.O. Box 351, Stuttgart, AR 72160 USA
^b Stuttgart National Aquaculture Research Center, P.O. Box 860, Stuttgart, AR 72160 USA

pcounce{at}comp.uark.edu

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
The large area of rice (Oryza sativa L.) production worldwide is critical to the well being of large numbers of the world's people. Yet for rice, the most important single plant species for human nutrition, there is not a widely used growth staging system. Despite good points of the published rice growth staging systems, none has been used widely for describing rice growth and development. Consequently, an objective growth staging system with enumeration adapted to cumulative leaf number (CLN) would improve communication among scientists, farmers, and educators. We propose a rice developmental staging system divided into three main phases of development: seedling, vegetative, and reproductive. Seedling development consists of four growth stages: unimbibed seed (S0), radicle and coleoptile emergence from the seed (S1, S2), and prophyll emergence from the coleoptile (S3). Vegetative development consists of stages V1, V2 ... VN; N being equal to the final number of leaves with collars on the main stem. Reproductive development consists of 10 growth stages based on discrete morphological criteria: panicle initiation (R0), panicle differentiation (R1), flag leaf collar formation (R2), panicle exertion (R3), anthesis (R4), grain length and width expansion (R5), grain depth expansion (R6), grain dry down (R7), single grain maturity (R8), and complete panicle maturity (R9). Assigning rice growth stages based on discrete morphological criteria will result in unambiguous growth-stage determination. For example, using this system, two people staging the same plant will arrive at the same growth stage. This is because the system exploits the presence or absence of distinct morphological criteria in a symbolic logic dichotomous framework that only permits yes or no answers.

Abbreviations: CLN, cumulative leaf number • IE, internode elongation

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
RICE GRAIN is a food staple for more people than foods obtained from any other single plant species. Major portions of the world obtain more than half of their daily dietary calories from rice. Consequently, rice research and its application potentially affects the well being of a large part of the world's human population.

Biological understanding and practical value of crop growth staging systems have been progressive and cumulative. Crop growth staging systems are meant to be an aid in information transfer for crop management. They can also aid scientists and others in observing, recording, and communicating critical crop growth data. Yet for rice, the most important single plant species for human nutrition, there is not a widely used growth staging system. We found four published systems for describing rice development: Zadoks et al. (1974), IRRI (1980), the BBCH system (Lancashire et al., 1991), and Haun (1973). Zadoks et al. (1974) is an adaptation of Feekes' (1941) scale (with 23 subdivisions) but further delineated. The IRRI (1980) scale is a 10-point system (0–9) with no subdivisions. The BBCH (Lancashire et al., 1991) system for rice is an adaptation of the Zadoks et al. (1974) scale. Consequently, the BBCH and Zadoks et al. scales are 99 and 110 point systems, respectively. Haun (1973) also described a wheat (Triticum aestivum L.) developmental system that has been applied to rice. Haun's system is enumerated into CLN. All four systems have strengths and all share problems related to enumeration of growth stages and criteria for the determination of the growth stage. Despite good points of the published rice growth staging systems, none has been used widely for describing rice growth and development.

Terms that have been used to describe plant developmental time include plastochron and phyllochron. Plant age can be expressed in a biologically meaningful way by the CLN produced on the main stem. The time interval between successive leaf initiations is called a plastochron (Langer, 1972). The problem with determining the plastochron is that the initiated leaves are not visible without microscopy. A phyllochron is the time interval between the same leaf developmental events of successive leaves (Rickman and Klepper, 1995; Wilhelm and McMaster, 1995; Nemoto et al., 1995).

The concept of plant age by CLN was implicitly recognized by Bonnet, Kepler, Leonardo da Vinci, and perhaps Aristotle (Jean, 1994). The incorporation of plant age (as determined by CLN) into developmental systems has been progressive. Feekes (1941) essentially ignored the delineation of vegetative growth into phytomers in his system for wheat. Higgins et al. (1964) reported on CLN as a means of expressing plant age. Hanway (1963, 1966) recognized that corn (Zea mays L.) develops by CLN but did not enumerate his stages by CLN. Rather, he stayed with the enumeration proposed by Feekes (1941). However, Hanway did recognize CLN to a degree in his corn system. Haun (1973) appears to have been the first to incorporate CLN into the enumeration of a crop growth staging system. Haun recognized the modular nature of vegetative development for wheat and allowed his enumeration to be set by the plant, that is by the CLN (x in Haun's system), rather than an arbitrary number (e.g., 10, 11, 99, or 110). The discrete aspect of Haun's wheat development system was combined with the continuous criteria of the partial development of elongating leaves. Fehr and Caviness explicitly recognized CLN and incorporated three important advances into their soybean [Glycine max (L.) Merr.] growth staging system:

1. They implicitly recognized that CLN, phyllochron, and plastochron are biological phenomenon not limited to grasses.

2. Since vegetative and reproductive development proceed simultaneously, the staging system should reflect this simultaneous development.

3. They provided dichotomous criteria for the beginning of their growth stages.

Fehr and Caviness, like Haun, allowed the enumeration of the vegetative growth stages to be determined by the plant rather than being imposed arbitrarily upon it. Vegetative development was delineated and determined simply by leaf number without attempting to determine subsequent leaf elongation. Consequently, two people independently examining one soybean plant using the Fehr and Caviness system will arrive at the same growth stage.

If incorporated into existing systems, a crop growth staging system based on plant morphogenesis, with each stage differentiated from another dichotomously, would facilitate consistent crop growth staging. For example, two people would arrive at one answer for the growth stage of one plant. The dichotomy referred to is the symbolic logic framework for phrasing questions. Primarily discrete criteria are employed because criteria determined by quantitative measurement (e.g., length and width) are plastic and consequently productive of equivocal growth stage determinations. An objective morphological criterion is either present or absent; thus, for the question of whether a plant is at a given growth stage, the answer is either yes or no.

There are several systems in place to express various stages of rice development. Some are adapted to a small area of land across which conditions are consistent enough to make applicable assumptions about plant growth and development. These assumptions do not hold true for a larger area of land. In the Arkansas, Louisiana, Mississippi, and Texas rice growing areas, the differentiation of the panicle into branches is coincident with the first internode to elongate much more than its own width. Therefore, in Arkansas the stage of growth is called internode elongation (IE). By splitting the culm in half lengthwise, the differentiating panicle is visible as well as the first elongated internode. This is the stage of development when the N demand by the developing panicle is relatively high and which the rice crop has been responsive to midseason N fertilization. The green ring is the dark green circle found by slicing across the vertical axis of the rice culm just below the closely stacked initiated final leaves of the culm and the initiating panicle. Now, logically, supplying N at green ring would provide adequate N for the soon-to-be differentiating panicle. Both green ring and IE are easily visible without magnification. Farmers, salesmen, extension personnel, and researchers in Louisiana and Arkansas are familiar with the terms green ring and IE, so these terms are valuable. The problem with both terms is that they are indirect guides to the actual events of interest — panicle initiation and differentiation. In some cases panicle differentiation can occur without IE. Clearly what is needed is a system for expressing the actual event rather than the indicator. The use of the terms green ring and IE to manage the rice crop is adequate within proscribed areas but inaccurate or irrelevant in others. Consequently, in some locations the terms panicle initiation and differentiation are employed for the sake of scientific precision. Moreover, while panicle initiation is an event at a point in time, panicle differentiation is a process through time. The term panicle differentiation refers to differentiation of the panicle branches.

The power of the local jargon and systems is that they are concise and only growth stages needed for management decisions are identified. Consequently, local systems are simple, short and rely on visible markers. However, when new management decisions are required, the short local systems must often be expanded to address the new problems. Also, application of research results useful to farmers, educators, and researchers across large geographical areas is often impossible because of imprecise growth stage expression that may mean one thing in one area and another elsewhere. Consequently, a precise, objective, and adaptive rice growth staging system is needed for present application and future needs of farmers, educators, and researchers.

The primary value of an objective and adaptive crop growth staging system is enhanced communication among farmers, consultants, crop insurers, scientists, teachers, and extension personnel. The central feature that allows meaningful communication is the ability to objectively determine the growth stage. The dichotomous feature assures that different people staging the same rice plant will obtain the same crop growth stage. The visibility of criteria is also critical to the system. It is more convenient in the field to observe things visible to the naked eye or with a small hand lens (10x magnification) rather than requiring a microscope. Consequently, plant morphological features visible with magnification less than or equal to 10x were favored as growth stage criteria. An adaptive rice growth staging system based on objective, visible, and discrete morphological developmental criteria can improve the usefulness of temperature time units with precise CLN time units.

	Morphogenesis

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
Rice morphological development can be divided into three phases: seedling, vegetative, and reproductive. These three phases are described in detail below. The late vegetative phase and the early reproductive phases occur simultaneously. The seedling and reproductive stages progress through a series of unique (occurring only once during development) events, whereas the vegetative stages progress through an iterative sequence of leaf developmental events. Thus, the phytomers are true examples of gnomonic development (incremental development in which each increment added to a structure results in a new structure resembling the original) (Jean, 1994).

	Seedling Development

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
To germinate, a dry rice seed must imbibe water. In germinating seeds, either a coleoptile or a radicle may emerge first. In dry-seeded conditions the radicle may emerge first, but in water-seeded conditions the coleoptile may emerge first. However, in at least some rice cultivars the coleoptile emerges before the radicle in dry-seeded conditions. A prophyll (rudimentary leaf) emerges from the coleoptile. This is followed by the emergence of the first leaf (one with a blade and sheath) above the prophyll. In low O₂ conditions, such as in water-seeded rice, the emergence of the radicle may occur after the emergence of the first complete leaf.

	Vegetative Development

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
Vegetative growth occurs in distinct, biological units of development time. The period between leaf collar formations on successive leaves is one measure of a phyllochron that is easily determined without magnification. We chose to employ successive collar formations for the vegetative growth stage determinations.

Vegetative development also occurs in distinct structural units called phytomers. A phytomer is the unit of vegetative development consisting of a leaf (blade and sheath) and its subtended node, internode, nodal roots, and tiller bud (Hoshikawa, 1989). Each complete (i.e., containing both sheath and blade) leaf on the main stem beginning with the first leaf can be marked as having completed elongation with collar formation. Note that collar formation is also one part of the completion of one phytomer or vegetative building block.

	Reproductive Development

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
Reproductive development begins when the shoot apex begins initiation of panicle structures. Subsequently, the panicle branches differentiate; the florets differentiate, including male and female organs as the panicle enlarges concurrently with the rest of the rice culm; microsporogenesis and megasporogenesis occur; the panicle emerges; anthesis occurs; the caryopsis elongates; the grain fills with starch; the grain ceases to fill; and the grain dries down. The nature of the grain continues to develop after harvest, leading to changes in the chemical and physical characteristics of the endosperm. Very detailed wheat apex development is provided by McMaster (1997) and detailed development of the rice plant is provided by Hoshikawa (1989) and by a later volume translated from Japanese (Matsuo and Hoshikawa, 1993).

	Purpose

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
The purpose of this paper is to present a uniform, adaptive system for expressing rice development.

	Materials and methods

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
The primary methods leading to the development of the system were (i) observing rice plants as they developed, (ii) noting dates of phenological events on the same plants, (iii) studying the literature on plant development and growth staging, and (iv) reflectively discussing these. Discussions were held with scientists from several disciplines to elucidate rice growth stages that were important to their discipline. Literature searches were made and an objective, adaptive rice growth staging system was presented and discussed on 4 Mar. 1998 at the Rice Technical Working Group in Reno, NV (Counce, 1998). Also, a workshop was held on 3 Sept. 1998 in Stuttgart, AR to demonstrate the system and to query participants about the system. There were several points raised in the discussion session that required further clarification either by literature searches or through experimental observation. The following experiments and observations were used to provide clarification where needed.

Seedling Growth Stages
Laboratory, growth chamber, and greenhouse experiments with water imbibition and seedling germination were used together with several years of field observations to delineate seedling stages. The procedure was to take 100 rice seeds of different cultivars and seed lots and place them in aereated tap water at a constant temperature of 25°C. Each day, seedlings with visible radicles and coleoptiles were counted.

Vegetative Growth Stages
Seeds of `Carolina Gold', `Drew', `Guichao2', `Lemont', `M11-131', `M202', and `Qiguizao' rice were planted on 12 and 13 May 1998 at the Rice Research and Extension Center near Stuttgart, AR on a Crowley silt loam soil (fine, smectitic, hyperthermic Typic Albaqualf). These cultivars and some characteristics are listed in Table 1 . Beginning on 21 May 1998, plants were tagged when the prophyll leaves began to emerge from the coleoptiles. The date of collar formation for the first leaf was noted. Subsequently, collar formation for each successive leaf on the main stem was noted. A group of the same varieties grown at the Stuttgart location were also grown at the Northeast Research and Extension Center near Keiser, AR on a Sharkey silty clay loam (very-fine, smectitic, thermic Chromic Epiaquert). At Keiser, rice was planted on 26 May 1998. On 23 July 1998, Drew, Lemont, and M202 were planted at the site near Stuttgart and notes were taken as for the earlier planting. On 8 Aug. 1998, Drew was planted at the site near Stuttgart and notes were taken as for the earlier plantings. Observations on selected plants were made Monday through Saturday until anthesis occurred. One day per week, plants were not observed and leaf emergence noted on the subsequent day was marked to denote that the actual date of collar formation could have been either of 2 d.

Reproductive Growth Stages
Examination of rice panicle and grain development has been carried out since 1989. In 1997, individual panicles and grains were examined during the course of their development to propose the staging system. Confirming observations were made in 1998 in the field.

	Results and discussion

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
Description of the Rice Crop Growth Staging System
We propose a rice developmental staging system divided into three main phases of development: seedling, vegetative, and reproductive.

The sequence of normally occurring seedling developmental events consists of four growth stages: unimbibed seed (S0), radicle and coleoptile emergence from the seed (S1, S2), and prophyll emergence from the coleoptile (S3). There are exceptions to the sequence of events presented. In some cases the rice coleoptile emerges from the seed first and in other cases the radicle emerges first. When either emerges alone then the growth stage is S1. When both have emerged, the growth stage is S2. If the prophyll emerges from the coleoptile before the radicle emerges from the seed, then the growth stage is S3. The prophyll is the first leaf to emerge, but it lacks a blade and a collar and consists only of the leaf sheaf. The seedling growth stages, illustrations, and morphological criteria for each growth stage are presented in Fig. 1 .

View larger version (20K): [in this window] [in a new window]   Fig. 1 Rice seedling growth stages with morphological markers. The sequence of normally occurring seedling developmental events is presented. There are exceptions to the sequence given. In some cases the rice coleoptile emerges from the seed first and in other cases the radicle emerges first. When either emerges alone the growth stage is S1. When both have emerged, the growth stage is S2. If the prophyll emerges from the coleoptile before the radicle emerges from the seed, the growth stage is S3; the prophyll is the first leaf to emerge, but it lacks a blade and collar and consists only of the leaf sheath

View larger version (12K): [in this window] [in a new window]   Fig. 2 External morphological structures of a V1 rice plant relative to the growth staging system

View larger version (46K): [in this window] [in a new window]   Fig. 3 Rice vegetative growth stages with morphological markers for a rice cultivar with 13 true leaves on the main stem. The number of vegetative growth stages varies with the number of true leaves on the main stem. VF denotes flag leaf and it follows that VF-n denotes the nth node before the flag leaf (V9–V13)

View larger version (58K): [in this window] [in a new window]   Fig. 4 Rice reproductive growth stages with morphological markers. Other authors have chosen to use the terms "physiological maturity" or "cessation of dry matter accumulation" (R7). We avoid these terms because for rice such determinations are difficult or impossible to make with any known morphological marker. The brown hull indicates the grain has begun to dry (R8 and R9)

View larger version (29K): [in this window] [in a new window]   Fig. 5 Time line for rice growth stages and morphological changes in the rice plant

Microsporogenesis in some situations is an important event for crop management. The criteria for determining microsporogenesis is continuous and not discrete. It normally occurs during the R2 growth stage. This could be a growth stage denoted by R2_ms. The criterion for Growth Stage R2_ms would be continuous, not discrete: elongation of the sheath of the flag leaf to the midpoint in the height of the leaf sheath of the preceding leaf (which is at vegetative Growth Stage VF) and Reproductive Growth Stage R2. Microsporogenesis is not always but often associated with the criterion proposed for R2_ms. To be certain of microsporogenesis, microscopic examination of the florets is required.

Expansion of the system to include quantitative or microscopic criteria may be useful for some applications. The meaningfulness of such expansions will be of limited value outside a small area in most cases.

Enumeration of a Crop
The growth stages refer to individual plants, main stems, or grains. It is useful to have a way to quantitatively express the stage of development for a field. Fehr and Caviness (1979) and others suggested enumeration of individuals in a population, and if more than 50% had advanced into the next growth stage, then the crop was reckoned to be in the next growth stage. Individual grain maturation in the panicle can occur in more than one grain simultaneously. To enumerate a field within seedling, vegetative, or reproductive growth stages, take the average of the growth stages for the plants staged. Note that field enumeration cannot be averaged across growth stage divisions (i.e., seedling, vegetative, or reproductive). The decimal part of the average indicates the tendency of the plants on average to advance to the next growth stage. For instance, if three plants were staged from one field and one plant was at V5, one at V7, and one at V8, the growth stage would be V6.7.

	Conclusions

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
A uniform system for expressing rice development was presented. The system employs dichotomously applied objective morphological criteria for growth stage determinations. Enumeration is adapted to the CLN of the plant's main stems. The system can be used to determine stage of growth in an objective, unequivocal manner so that communication of rice research results and producer practices can be facilitated.IRRI 1980

	ACKNOWLEDGMENTS

 
We thank Arkansas rice farmers for support of this project through check-off funds administered by the Arkansas Rice Research and Promotion Board. Illustrations were done by Angela Rosencrantz Henderson. We thank Bobby Kelly and Mark Poag for notes and observations. We thank Chuck Caviness, Mark Poag, James Gibbons, Graeme Batten, Gary McCauley, Laurie Lewin, Karen Moldenhaeur, John Robinson, Jim Stansell, John Bernhardt, Fleet Lee, Jim Hill, Stacey Roberts, Liu Gang, Richard Dunand, Jerry Ludwig and numerous others for discussion and suggestions. Reviewers for the paper provided valuable insights. We appreciate the previous research on growth staging which contributed greatly to our understanding.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 
Paper no. 99001 published with the approval of the Director, Agricultural Experiment Station, University of Arkansas, Fayetteville, AR 72701. This research was supported by a grant from the Arkansas Rice Research and Promotion Board.

Received for publication February 10, 1999.

	REFERENCES

TOP NOTES ABSTRACT INTRODUCTION Morphogenesis Seedling Development Vegetative Development Reproductive Development Purpose Materials and methods Results and discussion Conclusions REFERENCES

 

• Counce, P.A. 1998. Report on growth staging session. p. 9–10. In Proceedings of the 27th Rice Technical Working Group. Texas Agric. Exp. Stn., Texas A&M Univ., College Station.
• Feekes, W. 1941. De tarwe en haar milieu. Vers. XVII Tech. Tarwe Comm. Groningen, 560-1.
• Fehr, W.R., and C.E. Caviness. 1979. Stages of soybean development. Spec. Rep. 80. Iowa State Univ., Coop. Ext. Serv., Ames.
• Hanway J.J. Growth stages of corn (Zea mays L.). Agron. J. 1963;55:487-491.[Abstract/Free Full Text]
• Hanway, J.J. 1966. How a corn plant develops. Spec. Rep. 48. Iowa State Univ., Coop. Ext. Serv., Ames.
• Haun J.R. Visual quantification of wheat development. Agron. J. 1973;65:116-119.[Abstract/Free Full Text]
• Higgins J.J., Haun J.R., Koch E.J. Leaf development: Index of plant response to environmental factors. Agron. J. 1964;56:489-492.[Abstract/Free Full Text]
• Hoshikawa K. The growing rice plant: An anatomical monograph. Tokyo, Japan: Nobunkyo, 1989.
• IRRI. Standard evaluation system for rice. Los Banos, Philippines: IRRI, 1980.
• Jean R.V. Phyllotaxis: A systemic study of plant morphogenesis. Cambridge, UK: Cambridge University Press, 1994.
• Lancashire P.D., Bleiholder H., Van Den Boom T., Langeluddeke P., Stauss R., Weber E., Witzenberger A. A uniform decimal code for growth stages of crops and weeds. Ann. Appl. Biol. 1991;119:561-601.
• Langer R.H.M. How grasses grow. London: Edward Arnold, Ltd, 1972.
• Matsuo, T., and K. Hoshikawa. (ed.) 1993. Science of the rice plant. Vol. 1. (Morphology). Food and Agriculture Policy Reseach Center, Tokyo, Japan.
• McMaster G.S. Phenology, development and growth of the wheat (Triticum aestivum L.) shoot apex: A review. Adv. Agron. 1997;59:63-105.
• Nemoto K., Morita S., Baba T. Shoot and root development in rice related to the phyllochron. Crop Sci. 1995;35:24-29.
• Rickman R.W., Klepper B.L. The phyllochron: Where do we go in the future. Crop Sci. 1995;35:44-49.[Abstract/Free Full Text]
• Wilhelm W.W., McMaster G.S. Importance of the phyllochron in studying development and growth in grasses. Crop Sci. 1995;35:1-3.
• Zadoks J.C., Chang T.T., Konzak C.F. A decimal code for growth stages of cereals. Weed Res. 1974;14:415-421.

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