Abstract
Main conclusion
In maize, intrinsic hormone activities and sap fluxes facilitate organogenesis patterning and plant holistic development; these hormone movements should be a primary focus of developmental biology and agricultural optimization strategies.
Abstract
Maize (Zea mays) is an important crop plant with distinctive life history characteristics and structural features. Genetic studies have extended our knowledge of maize developmental processes, genetics, and molecular ecophysiology. In this review, the classical life cycle and life history strategies of maize are analyzed to identify spatiotemporal organogenesis properties and develop a definitive understanding of maize development. The actions of genes and hormones involved in maize organogenesis and sex determination, along with potential molecular mechanisms, are investigated, with findings suggesting central roles of auxin and cytokinins in regulating maize holistic development. Furthermore, investigation of morphological and structural characteristics of maize, particularly node ubiquity and the alternate attachment pattern of lateral organs, yields a novel regulatory model suggesting that maize organ initiation and subsequent development are derived from the stimulation and interaction of auxin and cytokinin fluxes. Propositions that hormone activities and sap flow pathways control organogenesis are thoroughly explored, and initiation and development processes of distinctive maize organs are discussed. Analysis of physiological factors driving hormone and sap movement implicates cues of whole-plant activity for hormone and sap fluxes to stimulate maize inflorescence initiation and organ identity determination. The physiological origins and biogenetic mechanisms underlying maize floral sex determination occurring at the tassel and ear spikelet are thoroughly investigated. The comprehensive outline of maize development and morphogenetic physiology developed in this review will enable farmers to optimize field management and will provide a reference for de novo crop domestication and germplasm improvement using genome editing biotechnologies, promoting agricultural optimization.
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Data availability statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
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Acknowledgements
We thank Prof. Gerhard Leubner and Chunqing Zhang for their encouragement and valuable comments on the first draft of this manuscript back in summer of 2018. We thank all the authors and colleagues whose work has been cited in our manuscript. We are grateful to the breeders and farmers in China who opened their farms so we could photograph the maize plants and organs. We would like to thank Editage for their professional English language editing. We would like to thank Professor Christine Beveridge from the ARC Centre for Plant Success in Nature and Agriculture for her encouragement on the manuscript and her foresight to use knowledge of plant physiological networks in the genomic prediction of crop phenotypes; her ideas helped us to greatly improve our manuscript. We acknowledge the editors and anonymous reviewers for their constructive comments and suggestions for the manuscript.
Funding
Partial financial support was received through grants from the Modern Agricultural Industry Technology System Innovation Team of Shandong Province (SDAIT-02-02) and the Taishan Industry Leading Talent program (LJNY201819).
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Box/Glossary
- Box 1|Glossary 1
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Brief definitions of common terms used to describe maize organ structures, morphological features, developmental characteristics, genetic regulation, and molecular interaction among others.
- Node
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In maize, this refers to a point structure, especially in the form of lump or swelling where one stem internode joins another from which the leaves or lateral branches and axillary buds grow.
- Tassel
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The inflorescence that develops from the stem/shoot apical meristem after all vegetative leaves are produced. It is located at the top of the plant and produces the male flowers that carry or shed pollen during reproduction.
- Ear
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The inflorescence located at the top of axillary branches, develo** from the axillary shoot apical meristem. It carries the female flowers and finally produces seed or grain.
- Meristem
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A group of stem cells located in the growing tips of shoots and roots which is the primary niche of plants that determine developmental patterns of vegetative and reproductive organs.
- Sex determination
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Also termed as the sex selection, this refers to the process in which organ primordia of the inappropriate sex-pistil primordia in the tassel florets and stamen primordia in the ear florets suffer arrest and abortion.
- Organogenesis
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The process by which initially formed zygote and meristematic cells consecutively grow to synthesize and produce endogenous hormone fluxes that subsequently control cell differentiation and meristem production of organ primordia.
- Agricultural optimization
-
This is a general description that refers to the process by which agricultural methods are improved to be more scientifically informed, efficient, and productive. Here, we use it to explain that our novel insights into maize developmental patterning will be helpful to move crop grain production and breeding practices from trial-and-error to scientifically informed methods.
- Endosperm
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The triploid nutritive tissue found in the seeds of flowering plants (angiosperms) which surrounds and nourishes the embryo as the seed germinates. The endosperm is derived from fertilization of the central cell (containing two polar nuclei) with one sperm cell contributed by a given pollen grain.
- Germination
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The process observed when crop seeding occurs in adequate field conditions (e.g. warm and moist soil) and the planted seed absorbs water and begins to grow. The radicle is the first part to begin elongation, eventually breaking through the seed coat (i.e. pericarp), growing from the swollen kernel, and rapidly elongating. The radicle is followed by the coleoptile with the enclosed plumule (embryonic plant), and then three to four lateral seminal roots.
- Coleoptile
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The coleoptile of maize seedling is a leaf-like structure that is attached to the coleoptilar node and is modified as a protective covering for the plumule of the miniature plant in the develo** kernel or the growing seedling where rapid growth is vital for successful seed germination and early seedling bud emergence.
- Collar
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A partial structure of one fully expanded leaf, the first part of which appears visually in the leaf back as a discolored line between the leaf blade and leaf sheath.
- Silks
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Stigmata of maize ear flowers. Pollens fallen into the silks, germinate on the silk tube, and move through the silk to reach the ovule.
- Husks
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Also referred to as the bracts of maize inflorescences (largely ears). The husk is an expanded sheath that surrounds the ear shoot with widely spaced veins. In some varieties, the husk has a leaf blade at the terminal end which is analogous to a leaf blade emerging from the sheath of the stem vegetative leaf.
- Kernel
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A maize kernel is the one-seeded fruit that develops from the ovule parts following double fertilization. The entire kernel in which the immature seed, consisting of embryo, endosperm, and remnants of seed coats and nucellus, is permanently covered with an adhering pericarp. When the mature kernel is shelled, the pedicel (i.e., flower stalk) commonly remains attached to the base of the kernel.
- Pericarp
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The colorless and/or transparent outer layer of the kernel, derived from the maternal ovule epidermis.
- Aleurone layer
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A specific triploid tissue acting as the outermost layer of cereal kernel/seed endosperm.
- Double fertilization
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In the reproductive process of typical flowering plants, the egg cell and central cell fuse with two sperm to (typically from the same pollen grain) produce a diploid embryo and an accessory triploid endosperm, respectively.
- Paramutation
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A locus-dependent epigenetic process first described in maize which can result in heritable changes in gene expression and trans-homologue interactions.
- Anthers
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A type of male organ structure of plant flowers, producing and shedding pollen grains.
- CC-type glutaredoxins
-
Glutaredoxins (GRXs) are a class of small glutathione-dependent oxidoreductases ubiquitously contained in the cells of most organisms. They can interact with NADPH and glutathione reductase to catalyze disulfide reductions of target proteins via dithiol or monothiol. According to the conserved amino acid sequences at their active sites, CPYC, CGFS, and CC, and thus plant GRXs are divided into CPYC-, CGFS-, and CC-type classes. The dithiol GRXs depend on a conserved CXXC motif in the active site and can reduce both general protein disulfides and mixed disulfides, while the monothiol GRXs containing a typical CXXS motif in the active site can only reduce mixed disulfides.
- G-protein
-
Also known as GTP-binding protein, this term refers to the family of heterotrimeric guanine nucleotide-binding regulatory proteins that are ubiquitously present in plants and animal cells and act essentially in transducing receptor-generated signals across the plasma membrane.
- Sink strength
-
In plants, the fruit and/or seed are considered sink organs that act as the receiver and reservoir of photosynthate, mineral nutrition, and water from the source organs (largely leaves and roots). The dry matter accumulation or yield of fruit or seed primarily relies on the influx from source organs and receiving rate or storage capacity of sink organs, which are termed ‘sink strength’. Common phytohormones, such as auxin, cytokinins, and GA play important roles in the regulation of plant sink strength.
- Sink-source balance
-
A term that reflects the equilibrium degree of sink and source organs, focusing on the crosstalk between the comprehensive absorption of sink organs and the overall assimilate production of source organs.
- MADS-box
-
These genes represent a large multigene family in vascular plants. The MADS-box/MADS-domain takes its name from the MINICHROMOSOME MAINTENANCE1 (MCM1) gene in yeast, AGAMOUS (AG) in Arabidopsis, DEFICIENS (DEF) in Antirrhinum, and SERUM RESPONSE FACTOR (SRF) in humans, encoding a variety of transcription factors that share a common or conserved DNA-binding/dimerization region and recognize similar target DNA sequences.
- Bleeding test
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A sample test by which the root pressure can be approximately evaluated according to the rate and discharge of sap outflow from the horizontal cut of plant stalk.
- Cas9
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In plants, to obtain transgene-free mutants and to stabilize the genomes of offspring plants, a clustered regularly interspaced short palindromic repeats (CRISPR)–associated protein nuclease that can be programmed by guide RNA (gRNA) sequences is recruited to create DNA double-strand breaks at specific genomic sequences, resulting in generation of stable gene-edited offspring plants. This CRISPR-associated protein 9 is termed Cas9.
- Box 2|Glossary 2
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Brief definitions of novel terms that are specifically used in this review to describe the maize growth process, life cycle, and life history.
- Preparatory stage
-
The stage in which the maternal haploid gametogenesis occurs. This stage is considered a preparation process for the double fertilization and zygote genesis, resulting in the formation of diploid progeny plants.
- Developmental stage
-
The stage when the maternal kernel develops from the initial ovule with very little inner material/fluid present and fertilizes germ into mature seed with fully developed embryo, endosperm, and other caryopsis structures. In the early period of this kernel developmental process, the newly formed zygote develops rapidly into a proper embryo with radicle, coleoptile, stem and leaves, and other embryonic structures. Thus, during the later period of this process a develo** miniature progeny plant is found within the develo** kernel. This stage is considered the early developmental stage of the offspring plant.
- Vegetative stage
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The stage that principally sustains the primordium formation and rapid growth of vegetative organs.
- Reproduction preparatory stage
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The stage in which both vegetative and reproductive organs undergo rapid development and growth, including stem and leaf morphogenesis, inflorescence development, flower formation, and haploid gametogenesis, making primary preparations for the following reproduction processes.
- Reproductive stage
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The stage in which embryos within the develo** maternal kernels undergo primary development and growth, becoming miniature offspring plants with a stem, leaves, and other essential embryonic organs. Therefore, this stage occurs when the maternal plant reproduces seeds or offspring.
- Apoptotic stage
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The stage when the maize plant meets the end of its life and undergoes organ decomposition and tissue apoptosis; disappearing into the environment.
- Classical life history
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The life process undergone by an organism in its diploid sporophytic phase, from the newly formed zygote to life end, descripting the conventional biological events or variations involved in growth, development, and reproduction.
- Holistic life history
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The process undergone by an organism from its sporogenesis to life end, including the gametogenesis and conventional biological events occurring throughout the diploid sporophytic phase.
- Genetic life history
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The process undergone by an organism that can sustain the organism to copy and transmit both its genomes and the epigenetic memory of its life experience to its offspring, occurring from the early stage of its life to the end.
- Genetic life cycle
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The process undergone by a type of organism, in which the organism can perform the transmission of all genetic information to its offspring, beginning from the early stage of the life course when the organism can gain or form epigenetic memory and restarting at the same life stage of its next generation.
- Crop agronomic life cycle
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The process undergone by crops in the field, reflecting the important agronomic traits of a generation individuals/plants and the growth and development courses of yield related organs.
- Crop agronomic life history
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The field growth processes of crops which describes the complete life course undergone by one crop plant in the field, focusing on the developmental courses and variations of important agronomic traits.
- Developmental life history
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The process undergone by an organism in the span from its gametophyte formation to life end, including the zygote genesis and the conventional biological events occurring throughout diploid sporophytic phase.
- Developmental life cycle
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The integrated process that includes both the life course of a type of organism occurring throughout its diploid sporophytic phase and the biological experience of its gametophytes before the double fertilization, beginning from the gametophyte formation of a generation and restarting at the same life stage of its next generation.
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Li, Q., Liu, N. & Wu, C. Novel insights into maize (Zea mays) development and organogenesis for agricultural optimization. Planta 257, 94 (2023). https://doi.org/10.1007/s00425-023-04126-y
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DOI: https://doi.org/10.1007/s00425-023-04126-y