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. 2023 Mar;73(1):3-45.
doi: 10.1270/jsbbs.22088. Epub 2023 Mar 29.

Genetic basis controlling rice plant architecture and its modification for breeding

Wakana Tanaka  1 , Takaki Yamauchi  2 , Katsutoshi Tsuda  3   4
Affiliations

Genetic basis controlling rice plant architecture and its modification for breeding

Wakana Tanaka et al. Breed Sci. 2023 Mar.

Abstract

The shoot and root system architectures are fundamental for crop productivity. During the history of artificial selection of domestication and post-domestication breeding, the architecture of rice has significantly changed from its wild ancestor to fulfil requirements in agriculture. We review the recent studies on developmental biology in rice by focusing on components determining rice plant architecture; shoot meristems, leaves, tillers, stems, inflorescences and roots. We also highlight natural variations that affected these structures and were utilized in cultivars. Importantly, many core regulators identified from developmental mutants have been utilized in breeding as weak alleles moderately affecting these architectures. Given a surge of functional genomics and genome editing, the genetic mechanisms underlying the rice plant architecture discussed here will provide a theoretical basis to push breeding further forward not only in rice but also in other crops and their wild relatives.

Keywords: growth and development; inflorescence; leaf; root; shoot; stem.

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Figures

Fig. 1.
Fig. 1.
Structure of shoot and root apical meristems in rice. (A) A rice seedling (Taichung65) one week after germination. Locations of shoot and root apical meristems detailed in (B) and (C) are shown with dotted boxes. (B) Confocal micrograph of the shoot apical meristem (SAM). The putative stem cell region is indicated in yellow color. (C) Confocal micrograph of the root apical meristem (RAM). The putative initial cell region is indicated in yellow color. The inset is an enlarged view of the quiescent center (QC). The exact number of QC cells is controversial. Bars = 50 μm.
Fig. 2.
Fig. 2.
Genetic model of meristem regulation. (A) Longitudinal section of the shoot apex. A dotted orange line indicates the shoot apical meristem (SAM). (B) Model of genetic interactions involved in the maintenance of SAM indeterminacy. (C) Model of genetic interactions involved in stem cell maintenance in the SAM. (D) Longitudinal section of a flower primordium at the early stage of its development. A dotted orange line indicates the early flower meristem (eFM). (E) Model of stem cell maintenance in the eFM. (F) Longitudinal section of a flower primordium at the late stage of its development. A dotted orange line indicates the final flower meristem (fFM). (G) Model of stem cell maintenance in the fFM. Dotted arrows and T-lines represent presumptive controls that have not yet been tested in rice. P1, plastochron one leaf primordium. Bars = 50 μm.
Fig. 3.
Fig. 3.
Structure of leaves in rice and regulators of its development. (A) A photograph illustrating the structure of a mature rice leaf. (B) A hand section of the marginal region of a leaf blade. (C) A hand section of the midrib. (D) A hand section of the central region of a leaf sheath. (E) The initial stage of leaf formation accompanied by KNOX down-regulation in P0. (F) Regulators along the adaxial-abaxial (purple) and medial-lateral (green and yellow) axes. (G) Regulators along the proximal-distal axis (proximal region: yellow, distal region: green, ligule: pink). Patterning processes shown on the left occur at the P3 stage, whereas the switch from cell division to cell elongation is likely to occur at P4 (right). LV: large vein, SV: small vein, BC: bulliform cell, SC: sclerenchyma, ME: mesophyll cell, XY: xylem, PH: phloem, BS: bundle sheath cell, CC: clear cell, V: vascular bundle, H: hairs. Bars = 20 μm.
Fig. 4.
Fig. 4.
Regulatory model of axillary bud formation and elongation. (A) Schematic representation of axillary bud formation and key genes involved in this process. A solid red line next to each gene indicates the period when gene expression was observed, whereas a dotted red line indicates the period when it is not known whether the gene is expressed or not. (B) Model of stem cell regulation during axillary bud formation. A dotted arrow and T-line represent presumptive controls that have not been clarified. (C) Model of axillary bud elongation. A dotted arrow and T-line represent presumptive controls that have not yet been demonstrated in rice. Hormones and nutrients that have positive and negative effects on tillering are colored in orange and blue, respectively. The effect of auxin colored in green depends on the context/condition of the bud.
Fig. 5.
Fig. 5.
Developmental processes of the stem and their regulators. (A) A tissue section at the vegetative shoot apex. A dotted line in yellow represents a putative unit of the stem and P3 leaf primordium. Orange dotted circles are nodal plates. (B) A schematic representation of the vegetative stems shown in (A). (C) A schematic representation of the elongating stem in the reproductive phase. (D) A photograph illustrating that internodes are the primary part contributing to stem elongation. (E and F) Regulatory pathways for the internode elongation (E) and the radial growth of the stem (F). Green asterisks represent genes/QTLs found in deepwater rice. Red asterisks are QTLs that promote stem radial growth.
Fig. 6.
Fig. 6.
Developmental processes of rice inflorescence and their regulators. (A and B) A panicle of a japonica cultivar Taichun65. A dashed box indicates the region magnified in (B). (C) Regulatory pathways in the inflorescence meristems at the reproductive transition. (D) Regulatory pathways at the branch meristem formation stages. Red asterisks represent genes or proteins whose natural variations are known to affect inflorescence architectures.
Fig. 7.
Fig. 7.
Fibrous root system of rice and the mechanisms of crown root initiation and maintenance. (A) A photograph illustrating the fibrous root system of rice. The inset photograph shows the lateral root (LR) that emerged from the crown root (CR). The scale bars are 5 cm and 100 μm (inset graph). (B) A tissue section of the stem node and the emerging crown root primordia (CRP). The scale bar is 50 μm. (C) A scheme of the stem node and the crown root (primordia). The yellow arrows indicate the auxin flow. (D) Auxin- and cytokinin-dependent regulatory networks during crown root initiation. Protein-protein interaction between OsERF3 and OsWOX11 might be not required for crown root initiation. (E) A tissue section of the apical part of the crown root. The inset graph shows the asymmetric cell divisions of cortex/endodermis initial cells (co/en) and cortical (co) and endodermal (en) cells. The scale bars are 50 μm and 5 μm (inset graph). The exact number of QC cells is controversial. (F) A scheme of the root apical meristem. The yellow arrow indicates the auxin flow. (G) Regulatory pathways of crown root maintenance. The dotted arrow indicates a lack of strong evidence which supports the interaction. PHB function is according to the analogy of Arabidopsis.
Fig. 8.
Fig. 8.
Regulators of crown root outgrowth, emergence and growth angle. (A) A scheme of the crown root outgrowth and its regulators. The yellow arrow indicates the auxin flow. (B) A scheme of the crown root emergence under flooding and its regulators. The blue arrow indicates the mechanical force originating from crown root outgrowth. (C) A scheme of the crown root growth angle in deep rooting and shallow rooting cultivars, and the regulators of root gravitropic response. The yellow arrows indicate the auxin flows and the thickness of the arrows indicates the abundance of auxin flow. PIN2 and PIN3 functions are according to the analogies of Arabidopsis.
Fig. 9.
Fig. 9.
Mechanisms of constitutive and inducible aerenchyma formation. (A) Cross-sections of the crown roots of rice seedlings grown under aerobic and low-oxygen conditions (low O2). The scale bars are 100 μm. ae; aerenchyma. (B) A scheme of the anatomical structures of the crown roots. The cortex is expanded and aerenchyma is induced under lox-oxygen conditions. ae; aerenchyma. (C) Regulatory pathways of constitutive aerenchyma formation under aerobic conditions and inducible aerenchyma formation under flooding (low-oxygen) conditions. The involvement of OsMT1s in inducible aerenchyma formation is postulated based on the reactive oxygen species (ROS) scavenging activity of the OsMT1 proteins and their expression patterns.
Fig. 10.
Fig. 10.
Regulation of S-type and L-type lateral root formations. (A) Tissue sections of the S-type and L-type lateral root primordia (LRP). The scale bars are 50 μm. (B) A scheme of the S-type and L-type lateral root primordia (LRP) formations and the key regulators of the size of lateral root primordia. (C) Molecular mechanisms that regulate LRP initiation in the pericycle of the crown roots and the auxin flux from the pericycle to the apical part of the LRP (left). Regulatory pathways that determine the size of LRP (right). Accumulation of auxin in the basal part of the LRP stimulates the increase of LRP size.
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