Maize LAZY1 Mediates Shoot Gravitropism and Inflorescence Development through Regulating Auxin Transport, Auxin Signaling, and Light Response

Dong, Zhaobin; Jiang, Chuan; Chen, Xiaoyang; Zhang, Tao; Ding, Lian; Song, Weibin; Luo, Huai‐Rong; Lai, Jinsheng; Chen, Huabang; Liu, Renyi; Zhang, Xiaolan; Jin, Weiwei

doi:10.1104/pp.113.227314

Cited by 137 publications

(164 citation statements)

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“…In the past years, several genes that determine rice tiller angle have been cloned and characterized (5)(6)(7)(8)(9). Some of them, for example LA1 and LPA1, are involved in shoot gravitropism and thus regulate tiller/branch angle in different plant species (5,9,32,33), indicating that shoot gravitropism is the key component dictating the proper positioning of shoot branches. Although the asymmetric distribution of auxin has long been regarded as the main factor that affects shoot gravitropism, the underlying molecular mechanism still remains to be elucidated.…”

Section: Discussionmentioning

confidence: 99%

Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis

Sang

Chen

Liu

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

137

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Tiller angle, a key agronomic trait for achieving ideal plant architecture and increasing grain yield, is regulated mainly by shoot gravitropism. Strigolactones (SLs) are a group of newly identified plant hormones that are essential for shoot branching/ rice tillering and have further biological functions as yet undetermined. Through screening for suppressors of lazy1 (sols), a classic rice mutant exhibiting large tiller angle and defective shoot gravitropism, we identified multiple SOLS that are involved in the SL biosynthetic or signaling pathway. We show that SL biosynthetic or signaling mutants can rescue the spreading phenotype of lazy1 (la1) and that SLs can inhibit auxin biosynthesis and attenuate rice shoot gravitropism, mainly by decreasing the local indoleacetic acid content. Although both SLs and LA1 are negative regulators of polar auxin transport, SLs do not alter the lateral auxin transport of shoot base, unlike LA1, which is a positive regulator of lateral auxin transport in rice. Genetic evidence demonstrates that SLs and LA1 participate in regulating shoot gravitropism and tiller angle in distinct genetic pathways. In addition, the SL-mediated shoot gravitropism is conserved in Arabidopsis. Our results disclose a new role of SLs and shed light on a previously unidentified mechanism underlying shoot gravitropism. Our study indicates that SLs could be considered as an important tool to achieve ideal plant architecture in the future. P lant shoot gravitropism is a process in which plants perceive gravity stimuli and reorient the direction of growth during the plant growth and development. Gravitropism is a dynamic process, including the perception of gravity, transduction of the corresponding information into a biochemical signal, transmission of the biochemical signal to a response site, and organ curvature (1). Genetic studies have disclosed that shoot endodermal cells act as statocytes for shoot gravitropism (2). Amyloplast sedimentation transduces the gravitropic signal and leads to auxin redistribution, resulting in a higher auxin level on the lower side than on the upper side (1, 3). Although auxin redistribution upon gravistimulation plays an important role in shoot gravitropism, the mechanism by which auxin regulates shoot gravitropism is not yet understood.In rice the tiller angle, which is defined as the angle between the tiller and main culm, plays a key role in determining rice plant architecture and thus grain yield (4). Several genes controlling the tiller angle have been identified previously in rice, including LAZY1 (LA1), TILLER ANGLE CONTROL1 (TAC1), PROSTRATE GROWTH1 (PROG1), and LOOSE PLANT ARCHITECTURE1 (LPA1) (5-9). Among these genes, LA1 and LPA1 are reported to regulate tiller angle through shoot gravitropism. In the la1 mutant, the polar auxin transport (PAT) is enhanced, and the lateral auxin transport is decreased, resulting in a disturbance of auxin asymmetric distribution in the shoot base and therefore the tiller-spreading phenotype of rice plants (5).Strigolactones (S...

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Section: Discussionmentioning

confidence: 99%

Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis

Sang

Chen

Liu

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

137

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“…Auxin was shown to regulate the establishment and propagation of the preligule band in maize plants with null alleles of liguleless1, liguleless2, and liguleless narrow (Moon et al 2013), and P-glycoprotein (PGP) genes interact with PIN genes to influence local auxin distribution (Blakeslee Mravec et al 2008). Furthermore, rice LAZY1, a polar auxin transport repressor, regulates rice tiller angle via shoot gravitropism (Li et al 2007;Dong et al 2013), and maize ZmCLA4, an ortholog of rice LAZY1, increases shoot gravitropism and leaf angle at elevated expression levels (Zhang et al 2014). Additional work will be necessary to determine the mechanism by which dw3 alleles regulate leaf angle.…”

Section: Discussionmentioning

confidence: 99%

Harnessing Genetic Variation in Leaf Angle to Increase Productivity of Sorghum bicolor

et al. 2015

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The efficiency with which a plant intercepts solar radiation is determined primarily by its architecture. Understanding the genetic regulation of plant architecture and how changes in architecture affect performance can be used to improve plant productivity. Leaf inclination angle, the angle at which a leaf emerges with respect to the stem, is a feature of plant architecture that influences how a plant canopy intercepts solar radiation. Here we identify extensive genetic variation for leaf inclination angle in the crop plant Sorghum bicolor, a C4 grass species used for the production of grain, forage, and bioenergy. Multiple genetic loci that regulate leaf inclination angle were identified in recombinant inbred line populations of grain and bioenergy sorghum. Alleles of sorghum dwarf-3, a gene encoding a P-glycoprotein involved in polar auxin transport, are shown to change leaf inclination angle by up to 34°(0.59 rad). The impact of heritable variation in leaf inclination angle on light interception in sorghum canopies was assessed using functionalstructural plant models and field experiments. Smaller leaf inclination angles caused solar radiation to penetrate deeper into the canopy, and the resulting redistribution of light is predicted to increase the biomass yield potential of bioenergy sorghum by at least 3%. These results show that sorghum leaf angle is a heritable trait regulated by multiple loci and that genetic variation in leaf angle can be used to modify plant architecture to improve sorghum crop performance.KEYWORDS leaf angle; crop modeling; sorghum canopy; bioenergy sorghum; dwarf-3; P-glycoprotein; auxin transport S USTAINABLY increasing the productivity of crops on land currently used for agriculture without depleting natural resources is a global priority (Foley et al. 2011;Drewry et al. 2014). Improving the efficiency with which plants intercept solar radiation is one means to sustainably improve crop productivity. Leaf angle, or leaf erectness, is a plant canopy parameter that has drawn considerable attention because of the predicted improvement in photosynthetic efficiency and reduction in plant stress afforded by the redistribution of solar radiation from upper to lower levels of canopies (Tollenaar and Wu 1999;Duvick 2005;Murchie et al. 2009;Zhu et al. 2010;Murchie and Reynolds 2012;Drewry et al. 2014;Mansfield and Mumm 2014). Performance improvements predicted by theoretical models are corroborated by positive correlations between small leaf angles and cereal crop yields; post-green revolution rice cultivars have smaller leaf inclination angles and higher yields relative to their pre-green revolution predecessors (Yoshida 1972;Sinclair and Sheehy 1999;Sakamoto et al. 2006), and modern maize is also characterized by small inclination angles as a consequence of selection for increased grain yield in breeding programs (Duvick 2005;Lee and Tollenaar 2007;Hammer et al. 2009;Tian et al. 2011;Mansfield and Mumm 2014).Despite the association of leaf angle with increased productivity, its g...

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“…Total RNA was isolated from tiller buds harvested as described for ChIP. For qRT-PCR analysis, cDNA was synthesized from DNase I-treated total RNA as described previously (55). SD was calculated among three biological replicates for each sample.…”

Section: Methodsmentioning

confidence: 99%

Ideal crop plant architecture is mediated by tassels replace upper ears1, a BTB/POZ ankyrin repeat gene directly targeted by TEOSINTE BRANCHED1

Dong

Unger-Wallace

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Axillary branch suppression is a favorable trait bred into many domesticated crop plants including maize compared with its highly branched wild ancestor teosinte. Branch suppression in maize was achieved through selection of a gain of function allele of the teosinte branched1 (tb1) transcription factor that acts as a repressor of axillary bud growth. Previous work indicated that other loci may function epistatically with tb1 and may be responsible for some of its phenotypic effects. Here, we show that tb1 mediates axillary branch suppression through direct activation of the tassels replace upper ears1 (tru1) gene that encodes an ankyrin repeat domain protein containing a BTB/POZ motif necessary for protein-protein interactions. The expression of TRU1 and TB1 overlap in axillary buds, and TB1 binds to two locations in the tru1 gene as shown by chromatin immunoprecipitation and gel shifts. In addition, nucleotide diversity surveys indicate that tru1, like tb1, was a target of selection. In modern maize, TRU1 is highly expressed in the leaf trace vasculature of axillary internodes, while in teosinte, this expression is highly reduced or absent. This increase in TRU1 expression levels in modern maize is supported by comparisons of relative protein levels with teosinte as well as by quantitative measurements of mRNA levels. Hence, a major innovation in creating ideal maize plant architecture originated from ectopic overexpression of tru1 in axillary branches, a critical step in mediating the effects of domestication by tb1.A xillary meristems are produced at the base of each new leaf and can have different fates depending on their positions within the plant. In maize, those found aboveground have a reproductive fate, while those found at the base of the plant can become long branches that are vegetative clones of the main shoot and are called tillers. These extra branches often compete for valuable resources such as light (1) and can have a negative impact on plant growth if produced in excess. Indeed, suppression of axillary branching through an increase in apical dominance is a commonly bred trait among many domesticated crop plants (2), including maize (Zea mays ssp. mays), which was domesticated from teosinte (Z. mays ssp. parviglumis), its wild ancestor. While there are multiple genetic pathways necessary for suppression of axillary bud production in plants (3-5), in maize, this process has been found to operate through a specialized pathway mediated by the teosinte branched1 (tb1) locus first identified by Charles Burnham over 50 y ago (6). tb1 loss of function mutants overproduce tillers and have long aerial branches tipped by male tassels that replace the normally female ears (7), indicating that it functions as a repressor of both axillary bud growth and inflorescence sexual fate (8). Previous quantitative trait locus studies mapping the genetic basis for differences in plant morphology between maize and teosinte showed that selection at the tb1 locus was responsible for the increase in apical dominance foun...

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Maize LAZY1 Mediates Shoot Gravitropism and Inflorescence Development through Regulating Auxin Transport, Auxin Signaling, and Light Response

Cited by 137 publications

References 106 publications

Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis

Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis

Harnessing Genetic Variation in Leaf Angle to Increase Productivity of Sorghum bicolor

Ideal crop plant architecture is mediated by tassels replace upper ears1, a BTB/POZ ankyrin repeat gene directly targeted by TEOSINTE BRANCHED1

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