Setaria Seed Life History - Agronomy Courses - Iowa State University

85 Pages·2013·1.33 MB·English

Weedy Setaria Seed Life History

Jack Dekker
Weed Biology Laboratory
Agronomy Department
Iowa State University
Ames, Iowa 50010
USA
Email: [email protected]

KEYWORDS: biological algorithms; bristly foxtail; communication theory; community
assembly; complex adaptive systems; complexity; emergent behavior; giant foxtail; green
foxtail; information theory; knotroot foxtail; phenotypic plasticity; plant model system; seed
biology; seed dormancy; seed germinability; seed germination; seed heteroblasty; seed
polymorphism; seedling emergence; seedling recruitment; self-organization; self-similarity;
Setaria faberi; Setaria geniculata; Setaria italica; Setaria pumila; Setaria verticillata; Setaria
viridis; Shannon communication system; somatic polymorphism; weed biology; weed model
system; yellow foxtail

Summary. The nature of weeds is a complex adaptive, soil-seed communication system. The
nature of weedy Setaria life history is an adaptable, changeable system in which complex
behaviors emerge when self-similar plant components self-organize into functional traits
possessing biological information about spatial structure and temporal behavior. The nature of
the weedy Setaria is revealed in the physical (morphological and genetic spatial structures) and
the phenomenal (life history behavior instigated by functional traits). Structural self-similarity in
morphology is revealed in seed envelope compartmentalization and individual plant tillering; in
genetics by local populations and Setaria species-associations forming the global
metapopulation. Behavioral self-organization is revealed in the self-pollenating mating system
controlling genetic novelty, seed heteroblasty blueprinting seedling recruitment, and phenotypic
plasticity and somatic polymorphism optimizing seed fecundity. The weedy Setaria phenotype
can be described in terms of the spatial structure of its seed and plant morphology, and by its
genotypes and population genetic structure. This spatial structure extends from the cells and
tissues of the embryo axes, the surrounding seed envelopes, the individual seed and then plant,
the local deme, and ending with the aggregation of local populations forming the global
metapopulation. Setaria plant spatial structure is the foundation for emergent life history
behavior: self-similar timing of life history processes regulated by functional traits expressed via
environment-plant communication. Temporal life history behavior begins in anthesis,
fertilization and embryogenesis; development continues with inflorescence tillering, seed
dispersal in space and time, and resumption of embryo growth with seedling emergence. Setaria
life history behavior is a Markov chain of irreversible (dormancy induction; seed dispersal,
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germination, seedling emergence, neighbor interactions) and reversible (seed after-ripening,
dormancy re-induction) processes of seed-plant state changes (flowering plants, dormant seed,
seed germination candidate, germinated seed, seedling) regulated by morpho-physiological traits
acting through environment-plant communication systems (environment-plant-seed, soil-seed).
Heritable functional traits are the physical reservoirs of information guiding life history
development, emergent behavior. Information contained in structural and behavioral traits is
communicated directly between soil environment and seed during development. Functional
traits controlling seed-seedling behavior are physical information that has evolved in ongoing
communication between organism and environment leading to local adaption. The consequence
of structural self-similarity and behavioral self-organization has been the evolution of a complex
adaptive seed-soil communication system. Weedy Setaria life history is represented in
algorithmic form as FoxPatch, a model to forecast seed behavior. The environment-biological
informational system with which weedy Setaria life history unfolds is represented in the soil-
seed communication system.

CONTENTS

1. The nature of weed seeds and seedlings
1.1 Weed complexity
1.2 Biological communication
1.3 The general nature of weeds, the specific nature of weedy Setaria
2. The nature of weedy Setaria seed-seedling life history
2.1 Seed-seedling life history
2.2 The nature of Setaria: spatial structure and temporal behavior
2.3 Setaria model system of exemplar species
3. Setaria spatial structure
3.1 Plant morphological structure
3.2 Plant genetic structure
4. Setaria seed-seedling life history behavior
4.1 Life history behaviors: functions, traits and information
4.2 Seed formation and dormancy induction
4.3 Seed rain dispersal
4.4 Seed behavior in the soil
4.5 Seedling recruitment
5. Setaria seed life history as complex adaptive soil-seed communication system
5.1 Forecasting Setaria seed behavior: FoxPatch
5.2 Setaria soil-seed communication system
5.3 Seed memory and adaptive evolution
6. References Cited

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1. THE NATURE OF WEED SEEDS AND SEEDLINGS

“Present knowledge of the behavior of invading species, both successful and
unsuccessful, suggests that it is in phases of germination and seedling establishment that
their success or failure is most critically determined and it would seem reasonable
therefore, to look particularly closely at seeds and seedlings of invading species. The
considerations set out in this paper lead one to expect that it is in properties such as seed
number, seed size, seed polymorphisms, and precise germination requirements that the
most sensitive reactions of a species to an alien environment are likely to occur.”
(Harper, 1964)

The nature of weeds is a complex adaptive system. Weed life history is an adaptable,
changeable system in which complex behaviors emerge as a consequence of structural self-
similarity and behavioral self-organization.
The nature of weeds is an environment-biology communication system. Biology is
information. Information comes via evolution, an ongoing exchange between organism and
environment. Information is physical. Biology is physical information with quantifiable
complexity.

1.1 WEED COMPLEXITY

"The plant population that is found growing at a point in space and time is the
consequence of a catena of past events. The climate and the substrate provide the
scenery and the stage for the cast of plant and animal players that come and go. The
cast is large and many members play no part, remaining dormant. The remainder act
out a tragedy dominated by hazard, struggle and death in which there are few
survivors. The appearance of the stage at any moment can only be understood in
relation to previous scenes and acts, though it can be described and, like a photograph
of a point in the performance of a play, can be compared with points in other
plays. Such comparisons are dominated by the scenery, the relative unchanging
backcloth of the action. It is not possible to make much sense of the plot or the action
as it is seen at such a point in time. Most of our knowledge of the structure and
diversity of plant communities comes from describing areas of vegetation at points in
time and imposing for the purpose a human value of scale on a system to which this
may be irrelevant." (Harper, 1977)

A complex adaptative system (CAS) is a dynamic network of many interacting adaptive
agents acting in parallel (Axelrod and Cohen, 1999). The overall system behavior is a result of a
huge number of decisions, made every moment, by many individual agents acting and reacting in
competition and cooperation to what other agents are doing, in which control is highly dispersed
and decentralized. A CAS is a complex, self-similar collectivity of interacting adaptive agents
with emergent and macroscopic properties. Complex adaptive systems are open, defining system
boundaries is difficult or impossible. CASs operate far from equilibrium conditions, a constant
flow of energy is needed to maintain the organization of the system. CASs are living, adaptable,
changeable systems in which complexity, self-similarity and self-organization occur.
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1.1.1 Complexity
Complexity arises in a system composed of many elements in an intricate arrangement.
The numerous elements interact with each other by which numerous relationships are formed
among the elements. The relationship among system parts is differentiated from other parts
outside of system. A key principle of CAS behavior and evolution is that the basic system units
are agents (e.g phenotypes, strategic traits, cells) which scan/sense/perceive their environment
(opportunity spacetime, Dekker, 2011b) and develop schema/plans/traits representing
interpretive and action rules (e.g. seed heteroblasty). These schema/plans/traits are subject to
change and evolution. Agents are a collection of properties, strategies and capabilities for
interacting with local opportunity and other agents. Agents and the complex system are
adaptable, with a high degree of adaptive capacity providing resilience to disturbance. The
number of elements in a CAS is large such that a conventional description is impractical, and
does not assist in understanding the system (e.g. Colbach et al., 2001a, b). A second key
principle of CAS behavior and evolution is that system order is emergent, not predetermined.
Emergence is the way complex systems and patterns arise out of a multiplicity of relatively
simple interactions. Interactions are non-linear: small causes can have large effects (e.g.
pleiotropy in triazine resistant plants; Dekker, 1992, 1993). Interaction is physical or involves
exchange of information. Systems emerge from the moment-to-moment decisions made by
many players choosing among very many options at each time (Waldrop, 1994). Emergence is
the arising of novel (even radical) and coherent structures, patterns, properties during process of
self-organization in complex systems. A third key principle of CAS behavior and evolution is
that system history is irreversible; the system future is unpredictable. All CASs have a history,
they evolve, and their past is co-responsible for their present behavior, a Markov process.
1.1.2 Self-Similarity, Self-Affinity
Complex adaptive systems exhibit self-similarity when a component, or an object of the
system is exactly or approximately similar to a part of itself. In complex adaptive weed systems
self-similarity is revealed in several ways. Self-similarity is expressed in phenotypic plasticity
within an individual plant in response to local opportunity. Plastic responses to local opportunity
includes variation in the numbers and architecture of the plant body. Similar modular plant units
are repeated at several levels of spatial organization: modular shoot branching or tillering, leaves
and photosynthesizing cells; modular root branches, roots, root hairs and absorptive cells. Self-
similar phenotypes are expressed in the temporal population structure of a species in a local
deme, as well as in the continuous interacting local-to-global populations of the species’
metapopulations. Phenotypic traits in the individual are self-similar in variants produced by
parent plants to achieve slightly different strategic roles in local adaptation (e.g. seed
heteroblasty). These strategic traits in turn are self-similar as preadaptations, exaptations, when
those phenotypic traits confront new evolutionary situations in which function can change.
1.1.3 Self-Organization, Self-Assembly

“… (there exists a) distinction between planned architecture and self-assembly.” “The
key point is that there is no choreographer and no leader. Order, organization, structure
– these all emerge as by-products of rules which are obeyed locally and many times
over, not globally. And that is how embryology works. It is done by local rules, at
various levels but especially the level of the single cell. No choreographer. No
conductor of the orchestra. No central planning. No architect. In the field of
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development, or manufacture, the equivalent of this kind of programming is self-
assembly.” (Dawkins, 2009)

Self-organization in complex adaptive systems is the process wherein a structure or
global pattern emerges in a system solely from numerous local parallel interactions among lower
level components. Self-organization is achieved by elements distributed throughout the system,
without planning imposed by a central authority or external coordinator. The rules specifying
interactions among components are executed using only local information (without reference to
global patterns). It relies on multiple interactions exhibiting strong dynamical non-linearity; it
may involve positive and negative feedback, and a balance of exploitation and exploration. Self-
organization is observed in coherence or correlation of the integrated wholes within the system
that maintain themselves over some period of time. There exists a global or macro property of
“wholeness” (Corning, 2002).

1.2 BIOLOGICAL COMMUNICATION

"What lies at the heart of every living thing is not a fire, not a warm breath, not a 'spark
of life'. It is information, words, instructions ... If you want to understand life, don't
think about vibrant, throbbing gels and oozes, think about information technology."
(Dawkins, 1986).

The nature of weeds is an environment-biology communication system. Biology is
information. Evolution itself embodies an ongoing exchange of information between organism
and environment. For biology, information comes via evolution; what evolves is information in
all its forms and transforms. Information is physical. Biology is physical information with
quantifiable (Kolmogorov) complexity. The gene is not the information-carrying molecule, the
gene is the information.
Information in biological systems can be studied. An important problem in science is to
discover another language of biology, the language of information in biological systems. "The
information circle becomes the unit of life. It connotes a cosmic principle of organization and
order, and it provides an exact measure of that." (Loewenstein, 1999). This information circle
for weedy plants is the predictable developmental events of the annual life history.
Information theory was developed by Claude E. Shannon (Shannon and Weaver, 1949) to
find fundamental limits on signal processing operations such as compressing data and on reliably
storing and communicating data. Since its inception it has broadened to find applications in
statistical inference, networks (e.g. evolution and function of molecular codes, model selection
in ecology) and other forms of data analysis. A communication system of any type (e.g.
language, music, arts, human behavior, machine) must contain the following five elements (E)
(figure 1):
A Shannon communication system includes these elements, as well as the concepts of
message and signal. A message is the object of communication; a vessel which provides
information, it can also be this information; its meaning is dependent upon the context in which
it is used. A signal is a function that conveys information about the behavior or attributes of
some phenomenon in communication systems; any physical quantity exhibiting variation in time
or variation in space is potentially a signal if it provides information from the source to the
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destination on the status of a physical system, or conveys a message between observers, among
other possibilities.

Figure 1. Schematic diagram of Shannon information communication system (Shannon and
Weaver, 1949).

Communication Element Description
1 Information source entity, person or machine generating the message (characters, math function)
2 Transmitter operates on the message in some way: it converts (encodes) the message to
produce a suitable signal
3 Channel the medium used to transmit the signal
4 Receiver inverts the transmitter operation: decodes message, or reconstructs it from the
signal
5 Destination the person or thing at the other end

CHANNEL
Information
Source Transmitter Receiver Destination
Message Signal Received Message
Signal
Noise
Source

1.3 THE GENERAL NATURE OF WEEDS, THE SPECIFIC NATURE OF WEEDY
Setaria

The nature of communities is revealed with a complete phenotype life history description
of each plant species in a local community. Local plant community structure and behavior is an
emergent property of its component species. Community dynamics emerges from the interacting
life histories of these self-similar, self-organizing, specific components. Understanding an
individual weed species in detail can provide the basis of comparison among and within weed
species of a local plant community. The challenge is to discover the qualities of each member of
the weed-crop community, the nature and variation of species traits used to exploit local
opportunity. These insights provide a deeper, specific, understanding of biodiversity responsible
for community assembly, structure and (in)stability.
It is in the nature of weedy Setaria to process ambient environmental information as a
communication system in the process of life history seizure and exploitation of local opportunity.
The setting of weed evolution, the stage upon which diversifying evolution takes place, is a local
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population of variable phenotypes of a weed species in a particular locality. The nature of a
particular locality is defined by the opportunity spacetime available to the weed population to
seize and exploit, to survive and reproduce. Opportunity spacetime for a population is the
locally habitable space for an organism at a particular time. It is defined by its available
resources (e.g. light, water, nutrients, gases), pervasive conditions (e.g. heat, terroir), disturbance
history (e.g. tillage, herbicides, frozen winter soil), and neighboring organisms (e.g. crops, other
weed species) with which it interacts (Dekker, 2011B). It is the local niche, the niche
hypervolume (Hutchison, 1957).
The weedy Setaria species-group provides an exemplar of widely distributed species
whose complex life history behavior arises from multiple interacting traits. The specific nature
of Setaria seed-seedling biology provides strong inferences of the nature of all weeds,
elucidating the range of adaptations used by individual species to seize and exploit opportunity in
agro-communities.

2. THE NATURE OF WEEDY Setaria SEED-SEEDLING LIFE HISTORY

The nature of weedy Setaria seed-seedling life history can be described as a complex
adaptive, soil-seed communication, system arising from its component functional traits.
Complex seed structures and behaviors emerge as a consequence of self-organization of self-
similar parts forming this adaptive soil-seed communication system. Functional traits controlling
seed-seedling behavior are physical information that have evolved in ongoing communication
between organism and environment leading to local adaption.
The nature of weedy Setaria life history emerges when self-similar plant components
self-organize into functional traits possessing biological information about spatial structure and
temporal behavior. Spatial plant structure extends through the morphological (embryo to plant)
and genetic (plant to metapopulation). Temporal life history behavior begins in
anthesis/fertilization and embryogenesis; development continues with inflorescence tillering,
seed dispersal in space and time, and resumption of embryo growth with seedling emergence.
The interaction of self-similar plant components leads to functionally adapted traits, self-
organization. These heritable functional traits are the physical reservoirs of information guiding
life history development, emergent behavior. Information contained in structural and behavioral
traits is communicated directly between seed and soil environment during development. The
specific nature of Setaria is elucidated in table 1.

2.1 SEED-SEEDLING LIFE HISTORY

2.1.1 Threshold Events
Several discrete, threshold events characterize Setaria summer annual life history. These
threshold events provide time points allowing individual comparison in the elucidation of
development. The threshold life history events begin and end with successful fertilization,
continues with seed abscission, germination, and seedling emergence when the new vegetative
plant develops to fertilization of new progeny.

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Table 1. Plant structure (spatial, temporal) and emergent behavior examples of self-similar
components, self-organization functional traits, and communication-information in the life
history of weedy Setaria.

Self-Organization: Biological Emergent
Self-Similar Components Functional Traits Information Behavior
SPATIAL STRUCTURE
embryo
induction of
aleurone
differential
layer
dormancy-
seed caryopsis somatic polymorphism
germinability
envelopes coat
capacity in
hull environment- individual seeds of
glumes plant-seed inflorescence
Morphological seed communication
spikelet system
Plant inflorescence fascicle  somatic polymorphism
Structure panicle light capture
primary  phenotypic plasticity architecture
tiller 2
3

individual plant
local population (deme) control of genetic
self-pollination mating system gene flow
Genetic intra-specific variants novelty
communication
species associations polyploidization speciation trait dispersal for
system
meta-populations trait reservoir local adaptation
TEMPORAL STRUCTURE
time of embryogenesis of
seed germination heteroblasty: environment-
individual seeds on heterogeneous
Seed differential development: hull, plant-seed
inflorescence seed germinability
formation placental pore, TACL membrane; communication
time of tillering inflorescence capacity
oxygen scavenger protein system
branching
time of abscission of invasion and colonization seed dispersal in
Seed dispersal
individual seeds space
Life  hull topography: water film  seed dispersal in
History oxygenation time
Behavior Seed pool
behavior in  placental pore: water film soil-seed  annual
individual seeds from several
soil channel oxygen dormancy-
inflorescences, plants, years
communication germination

 TACL membrane: O transport system cycling in soil
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locally adapted
Seedling
 oxygen scavenger: embryo O emergence
emergence 2
regulation patterns
Self-Similar Components Self-Organization: Functional Biological Emergent
Traits Information Behavior

2.1.2 Germination and Seedling Emergence
One of the most important events in a plant's life history is the time of seed germination
and seedling emergence, the resumption of embryo growth and plant development. Emergence
timing is crucial, it is when the individual plant assembles in the local community and begins its
struggle for existence with neighbors. Resumption of growth at the right time in the community
allows the plant to seize and exploit local opportunity at the expense of neighbors, allowing
development to reproduction and replenishment of the local soil seed pool at abscission. Soil
seed pools are the source of all future local annual weed infestations, and the source of enduring
occupation of a locality.
Community assembly of crops and weeds in agroecosystems, and its consequences, is a
complex set of phenomena (Dekker et al., 2003). Accurate predictions of the time of weed
interference, weed control tactic timing, crop yield losses due to weeds, and replenishment of
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weed seed to the soil seed pool, require information about how agricultural communities
assemble and interact. Despite attempts at description (e.g. Booth and Swanton, 2002), little is
known about the rules of community assembly. Their elucidation may remain an empirically
intractable problem.
Despite this, there exist two opportunities to understand agroecosystem community
assembly during the recruitment phase (e.g. seedling emergence) that predicate future
interactions with other plants. The first advantage derives from the annual disturbance regime in
agricultural fields that eliminates above ground vegetation (e.g. winter kill, tillage including
seedbed preparation, early season herbicide use). Understanding community assembly is most
tractable when starting each growing year with a field barren of above-ground vegetation and
possessing only dormant underground propagules (e.g soil seed and bud pools), a typical
situation in much of world agriculture.
The second advantage derives from the observation that the time of emergence of a
particular plant from the soil relative to its neighbors (i.e. crops, other weeds) is the single most
important determinate of subsequent weed control tactic use, competition, crop yield losses and
weed seed fecundity. Seedling recruitment is the first assembly step in these disturbed
agricultural communities, and is therefore the foundation upon which all that follows is based.
Information predicting recruitment therefore may be the single most important life history
behavior in weed management.

2.2 THE NATURE OF Setaria: SPATIAL STRUCTURE AND TEMPORAL BEHAVIOR

Any complete description of an organism includes the concept of phenotypic function,
which consists of two universes: the physical (the quantitative, formal structure) and the
phenomenal (qualities that constitute a 'world') (Sacks, 1998). The nature of Setaria weed seeds
and seedlings is presented in this review as the story of plant spatial structure (genetic,
morphological) and temporal life history behaviors, instigated by functional traits, and resulting
in local adaptation and biogeography. The weedy phenotype can be described in terms of its
morphological structure, the embryo and specialized structures forming the seed, and the self-
similar shoot tiller architecture on which reproductive inflorescences arise. The individual, self-
similar seeds, form local populations (the deme) which aggregate, self-organize, into the global
metapopulation. The genetic and morphological structure provides an enduring foundation for
the evolution of life history behavioral adaptation: plant functions, functional traits and
regulation of function. The behavioral regulation of the Setaria phenotype is an emergent
property arising from the interaction of several morpho-physiological seed compartments
(embryo, caryopsis, hull, spikelet, fascicle, inflorescence tiller). The emergent property of these
interacting, self-organizing, self-similar components is seed heteroblasty: the abscission of
individual seeds from a panicle, each with different inherent dormancy-germination capacities.
Seed heteroblasty is the physical information forming memory of successful past seedling
emergence times appropriate to a locality. It is the hedge-bet for seizing and exploiting future
opportunity spacetime.

2.3 Setaria MODEL SYSTEM OF EXEMPLAR SPECIES

"One major biological question is how different species become unique organisms. To
understand the origins of adaptation ... it is particularly useful to investigate multiple
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species, especially when they have independently evolved an ability to prosper under
similar environmental conditions. With the sequencing of the Setaria genome,
evolutionary geneticists now have an annual, temperate, C , drought and cold tolerant
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grass that they can comprehensively compare to other plants that have or have not
evolved these adaptations ... particular traits were targeted ... for biotechnical
improvement, namely drought tolerance, photosynthetic efficiency and flowering
control. With a completed genome sequence, the door is now open for further
development of Setaria as a model plant. This model can be applied to understanding
such phenomena as cell wall composition, growth rate, plant architecture and input
demand that are pertinent to the development of biofuel crops. In addition to its use as a
panicoid model for switchgrass, pearl millet, maize and Miscanthus, Setaria has the
model characteristics that will encourage its development as a study system for any
biological process, with pertinence to the entire plant kingdom and beyond." (Bennetzen
et al., 2012)

The weedy Setaria species-group (green foxtail, S. viridis; bristly foxtail, S. verticillata;
giant foxtail, S. faberi; yellow foxtail, S. pumila; knotroot foxtail, S. geniculata) (Rominger,
1962) is presented herein as a weed exemplar of a complex adaptive, soil-seed communication,
system. The nature of the weedy Setaria species-group as a complex communication system is
an exemplar in the sense of Kuhn (1962), "... concrete problem-solutions ...".
Setaria provides a model system for seed germination, plant architecture, genome
evolution, photosynthesis, and bioenergy grasses and crops. It is used "... as an experimental
crop to investigate many aspects of plant architecture, genome evolution, and physiology in the
bioenergy grasses ... whose genome is being sequenced by the Joint Genome Institute (JGI) of
the Department of Energy.", "... it is closely related to the bioenergy grasses switchgrass
(Panicum virgatum), napiergrass (Pennisetum purpureum), and pearl millet (Pennisetum
glaucum), yet is a more tractable experimental model because of its small diploid genome ... and
inbreeding nature." (Doust et al., 2009). Setaria provides a "... potentially powerful model
system for dissecting C photosynthesis ..." (Brutnell et al., 2010) and "... provide novel
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opportunities to study abiotic stress tolerance and as models for bioenergy feedstocks." (Li and
Brutnell, 2011). A high-quality reference genome sequence has been generated for Setaria
italica and Setaria viridis (Bennetzen et al., 2012).
The weedy Setaria species-group (Darmency and Dekker, 2011; Dekker, 2003, 2004a;
Dekker et al., 2012a, 2012b), S. glauca and S. verticillata (Steel et al., 1983), and S. viridis,
(Douglas et al., 1985) have been reviewed.
The author has collected a very large (more than 3000 accessions) Setaria spp.-gp.
germplasm collection stored in the Weed Biology Laboratory, Agronomy Department, Iowa
State University, Ames. It includes Japanese salt-tolerant germplasm (e.g Dekker and Gilbert,
2008), herbicide resistant biotypes (e.g. Thornhill and Dekker, 1993), systematic pre-transgenic
crop era USA (notably Iowa) collections, and north temperate world populations (e.g. Wang et
al., 1995a, b).

3. Setaria SPATIAL STRUCTURE

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