The IDD Transcription Factors:Their Functions in Plant Development and Environmental Response

INDETERMINATE-DOMAIN proteins(IDDs)are a plant-specific transcription factor family characterized by a conserved ID domain with four zinc finger motifs.Previous studies have demonstrated that IDDs coordinate a diversity of physiological processes and functions in plant growth and development,including floral transition,plant architecture,seed and root development,and hormone signaling.In this review,we especially summarized the latest knowledge on the functions and working models of IDD members in Arabidopsis,rice,and maize,particularly focusing on their role in the regulatory network of biotic and abiotic environmental responses,such as gravity,temperature,water,and pathogens.Understanding these mechanisms underlying the function of IDD proteins in these processes is important for improving crop yields by manipulating their activity.Overall,the review offers valuable insights into the functions and mechanisms of IDD proteins in plants,providing a foundation for further research and potential applications in agriculture.

PROG1 acts upstream of LAZY1 to regulate rice tiller angle as a repressor

Rice tiller angle,as a component of plant architecture,affects rice grain yield via plant density.However,the molecular mechanism underlying rice tiller angle remains elusive.We report that the key domestication gene PROSTRATE GROWTH 1(PROG1)controls rice tiller angle by regulating shoot gravitropism and LAZY1(LA1)-mediated asymmetric distribution of auxin.Acting as a transcriptional repressor,PROG1 negatively regulates the expression of LA1 in light-grown rice seedlings.Overexpression of LA1 partially rescued the larger tiller angle of the PROG1 complementation transgenic plant(prog1-D).Double-mutant analysis showed that PROG1 acts upstream of LA1 to regulate shoot gravitropism and tiller angle.Mutation of Suppressors of lazy1(SOL1),encoding DWARF3(D3)acting in the strigolactone signal pathway,suppressed the large tiller angle of prog1-D by rescuing the transcription of LA1.The discovery of a light-sensitive PROG1-LA1 transcription regulatory module controlling rice shoot gravitropism and tiller angle sheds light on the genetic control of rice tiller angle.

A Botanist’s Cognitive View on Plant Growth: Cross-Talk between Developmental and Sensitivity Networks

An alteration in plant phenotypes assisted by their responses to the environmental stimuli (=tropism) has been fundamental to understand the “plant sensitivity ” that plays a crucial role in plants’ adaptive success. Plants succeed through the deployment of moderators controlling polar auxin-transport determining organ bending. Stimulus-specific effectors can be synthesized by the outer peripheral cells at the bending sites where they target highly conserved cellular processes and potentially persuade the plant sensitivity at large. Remarkably, the peripheral cells require different time-intervals to achieve the threshold expression-levels of stimulus-specific molecular responders. After stimulus perception, tropic curvatures (especially at growing root-apices) are duly coordinated via integrated chemical and electrical signalling which is the key to cellular communications. Thus, the acquired phenotypic alterations are the perplexed outcome of plant’s developmental pace, complemented by the sensitivity. A novel aspect of this study is to advance our understanding of plant developmental-programming and the extent of plant-sensitivity, determining the plant growth and their future applications.

Brassinosteroid-regulated plant growth and development and gene expression in soybean

Brassinosteroids(BRs) are endogenous phytohormones that play important roles in regulating plant growth and development.In this study, we evaluated the effects of brassinolide(BL, one of the active BRs) on soybean and identified roles of the hormone in regulating multiple aspects of plant growth and development.BL application promoted hypocotyl and epicotyl elongation in the light but blocked epicotyl elongation in the dark.High levels of castasterone and BL accumulated in light-grown plants.BL disrupted shoot negative gravitropism, whereas gibberellin did not.BL delayed leaf senescence.Transcriptome analysis showed that BL induced cell wall-modifying genes and auxin-associated genes but suppressed a class of WRKY genes involved in senescence and stress responses,showing the complex roles of BRs in multiple biological processes.

Identification of a Gravitropism-Deficient Mutant in Rice

A gravitropism-deficient mutant M96 was isolated from a mutant bank, generated by ethyl methane sulfonate(EMS) mutagenesis of indica rice accession ZJ100. The mutant was characterized as prostrate growth at the beginning of germination, and the prostrate growth phenotype ran through the whole life duration. Tiller angle and tiller number of M96 increased significantly in comparison with the wild type. Tissue section observation analysis indicated that asymmetric stem growth around the second node occurred in M96. Genetic analysis and gene mapping showed that M96 was controlled by a single recessive nuclear gene, tentatively termed as gravitropism-deficient M96(gd M96), which was mapped to a region of 506 kb flanked by markers RM5960 and In Del8 on the long arm of chromosome 11. Sequencing analysis of the open reading frames in this region revealed a nucleotide substitution from G to T in the third exon of LOC_Os11g29840. Additionally, real-time fluorescence quantitative PCR analysis showed that the expression level of LOC_Os11g29840 in the stems was much higher than in the roots and leaves in M96. Furthermore, the expression level was more than four times in M96 stem than in the wild type stem. Our results suggested that the mutant gene was likely a new allele to the reported gene LAZY1. Isolation of this new allele would facilitate the further characterization of LAZY1.

The chloroplast-localized protein LTA1 regulates tiller angle and yield of rice

Plant architecture strongly influences rice grain yield.We report the cloning and characterization of the LTA1 gene,which simultaneously controls tiller angle and yield of rice.LTA1 encodes a chloroplastlocalized protein with a conserved YbaB DNA-binding domain,and is highly expressed in photosynthetic tissues including leaves and leaf sheaths.Disrupting the function of LTA1 leads to large tiller angle and yield reduction of rice.LTA1 affects the gravity response by mediating the distribution of endogenous auxin,thereby regulating the tiller angle.An lta1 mutant showed abnormal chloroplast development and decreased chlorophyll content and photosynthetic rate,in turn leading to reduction of rice yield.Our findings shed light on the genetic basis of tiller angle and provide a potential gene resource for the improvement of plant architecture and rice yield.

Characterization of wavy root 1,an agravitropism allele,reveals the functions of OsPIN2 in fine regulation of auxin transport and distribution and in ABA biosynthesis and response in rice(Oryza sativa L.)

Root system architecture is influenced by gravity.How the root senses gravity and directs its orientation,so-called gravitropism,is not only a fundamental question in plant biology but also theoretically important for genetic improvement of crop root architecture.However,the mechanism has not been elucidated in most crops.We characterized a rice agravitropism allele,wavy root 1(war1),a loss-of-function allele in OsPIN2,which encodes an auxin efflux transporter.With loss of OsPIN2 function,war1 leads to altered root system architecture including wavy root,larger root distribution angle,and shallower root system due to the loss of gravitropic perception in root tips.In the war1 mutant,polar auxin transport was disrupted in the root tip,leading to abnormal auxin levels and disturbed auxin transport and distribution in columella cells.Amyloplast sedimentation,an important process in gravitropic sensing,was also decreased in root tip columella cells.The results indicated that OsPIN2 controls gravitropism by finely regulating auxin transport,distribution and levels,and amyloplast sedimentation in root tips.We identified a novel role of OsPIN2 in regulating ABA biosynthesis and response pathways.Loss of OsPIN2 function in the war1 resulted in increased sensitivity to ABA in seed germination,increased ABA level,changes in ABA-associated genes in roots,and decreased drought tolerance in the seedlings.These results suggest that the auxin transporter OsPIN2 not only modulates auxin transport to control root gravitropism,but also functions in ABA signaling to affect seed germination and root development,probably by mediating crosstalk between auxin and ABA pathways.

Arabidopsis Phytochrome D Is Involved in Red Light-Induced Negative Gravitropism of Hypocotyles

The phytochrome gene family, which is in Arabidopsis thaliana, consists of phytochromes A-E（phyA to phyE）, regulates plant responses to ambient light environments. PhyA and phyB have been characterized in detail, but studies on phyC to phyE have reported discrepant functions. In this study, we show that phyD regulates the Arabidopsis gravitropic response by inhibiting negative gravitropism of hypocotyls under red light condition. PhyD had only a limited effect on the gravitropic response of roots in red light condition. PhyD also enhanced phyB-regulated gravitropic responses in hypocotyls. Moreover, the regulation of hypocotyl gravitropic responses by phyD was dependent upon the red light fluence rate.

The AFB1 auxin receptor controls the cytoplasmic auxin response pathway in Arabidopsis thaliana

The phytohormone auxin triggers root growth inhibition within seconds via a non-transcriptionalpathway.Among members of the TIR1/AFB auxin receptor family,AFB1 has a primary role in this rapidresponse. However, the unique features that confer this specific function have not been identified.Here we show that the N-terminal region of AFB1, including the F-box domain and residues thatcontribute to auxin binding,is essential and sufficient for its specific role in the rapid response. Substitutionof the N-terminal region of AFB1 with that of TIR1 disrupts its distinct cytoplasm-enriched localizationand activity in rapid root growth inhibition by auxin. Importantly, the N-terminal region of AFB1 isindispensable for auxin-triggered calcium influx, which is a prerequisite for rapid root growth inhibition.Furthermore, AFB1 negatively regulates lateral root formation and transcription of auxin-induced genes,suggesting that it plays an inhibitory role in canonical auxin signaling. These results suggest that AFB1may buffer the transcriptional auxin response, whereas it regulates rapid changes in cell growth thatcontributeto rootgravitropism.

Brassinosteroids Regulate Root Growth, Development, and Symbiosis

Brassinosteroids （BRs） are natural plant hormones critical for growth and development. BR-deficient or signaling mutants show significantly shortened root phenotypes. But for a long time, it was thought that these phenotypes were solely caused by reduced root cell elongation in the mutants. Functions of BRs in regulating root development have been largely neglected. Recent detailed analyses, however, revealed that BRs are not only involved in root cell elongation but are also involved in many aspects of root development, such as maintenance of meristem size, root hair formation, lateral root initiation, gravitropic response, mycorrhiza formation, and nodulation in legume species. In this review, current findings on the functions of BRs in mediating root growth, development, and symbiosis are discussed.

Negative phototropism of rice root and its influencing factors

Some characteristics of the rice (Oryza sativa L.) root were found in the experiment of unilaterally irradiating the roots which were planted in water: (ⅰ) All the seminal roots, adventitious roots and their branched roots bent away from light, and their curvatures ranged from 25° to 60°. The curvature of adventitious root of the higher node was often larger than that of the lower node, and even larger than that of the seminal root. (ⅱ) The negative phototropic bending of the rice root was mainly due to the larger growth increment of root-tip cells of the irradiated side compared with that of the shaded side. (ⅲ) Root cap was the site of light perception. If root cap was shaded while the root was irradiated the root showed no negative phototropism, and the root lost the characteristic of negative phototropism when root cap was divested. Rice root could resume the characteristic of negative phototropism when the new root cap grew up, if the original cells of root cap were well protected while root cap was divested. (ⅳ) The growth increment and curvature of rice root were both influenced by light intensity. Within the range of 0-100μmol@m-2@s-1, the increasing of light intensity resulted in the decreasing of the growth increment and the increasing of the curvature of rice root. (ⅴ) The growth increment and the curvature reached the maximum at 30℃ with the temperature treatment of 10-40℃. (ⅵ) Blue-violet light could prominently induce the negative phototropism of rice root, while red light had no such effect. (ⅶ) The auxin (IAA) in the solution, as a very prominent influencing factor, inhibited the growth, the negative phototropism and the gravitropism of rice root when the concentration of IAA increased. The response of negative phototropism of rice root disappeared when the concentration of IAA was above 10 mg@L-1.

Seven Things We Think We Know about Auxin Transport

Polar transport of the phytohormone auxin and the establishment of localized auxin maxima regulate em- bryonic development, stem cell maintenance, root and shoot architecture, and tropic growth responses. The past decade has been marked by dramatic progress in efforts to elucidate the complex mechanisms by which auxin transport regulates plant growth. As the understanding of auxin transport regulation has been increasingly elaborated, it has become clear that this process is involved in almost all plant growth and environmental responses in some way. However, we still lack information about some basic aspects of this fundamental regulatory mechanism. In this review, we present what we know （or what we think we know） and what we do not know about seven auxin-regulated processes. We discuss the role of auxin transport in gravitropism in primary and lateral roots, phototropism, shoot branching, leaf expansion, and venation. We also discuss the auxin reflux/fountain model at the root tip, flavonoid modulation of auxin transport processes, and outstanding aspects of post-translational regulation of auxin transporters. This discussion is not meant to be exhaustive, but highlights areas in which generally held assumptions require more substantive validation.

OsBRXL4 Regulates Shoot Gravitropism and Rice Tiller Angle through Affecting LAZY1 Nuclear Localization

Rice tiller angle is a key agronomic trait that contributes to ideal plant architecture and grain production.LAZY1 (LA1) was previously shown to control tiller angle via affecting shoot gravitropism,but the underlying molecular mechanism remains largely unknown.In this study,we identified an LA1-interacting protein named Brevis Radix Like 4 (OsBRXL4).We showed that the interaction between OsBRXL4 and LA1 occurs at the plasma membrane and that their interaction determines nuclear localization of LA1.We found that nuclear localization of LA1 is essential for its function,which is different from AtLA1,its Arabidopsis ortho.log.Overexpression of OsBRXL4 leads to a prostrate growth phenotype,whereas OsBRXLs RNAi plants,in which the expression levels of OsBRXLI,OsBRXL4,and OsBRXL5 were decreased,display a compact phenotype.Further genetic analysis also supported that OsBRXL4 controls rice tiller angle by affecting nuclear localization of LA1.Consistently,we demonstrated that OsBRXL4 regulates the shoot gravitropism through affecting polar auxin transport as did LA1.Taken together,our study not only identifies OsBRXL4 as a regulatory component of rice tiller angle but also provides new insights into genetic regulation of rice plant architecture.

An Overview of the Biology of Reaction Wood Formation

Reaction wood possesses altered properties and performs the function of regulating a tree＇s form, but it is a serious defect in wood utility. Trees usually develop reaction wood in response to a gravistimulus. Reaction wood in gymnosperms is referred to as compression wood and develops on the lower side of leaning stems or branches. In arboreal, dicotyledonous angiosperms, however, it is called tension wood and is formed on the upper side of the leaning. Exploring the biology of reaction wood formation is of great value for the understanding of the wood differentiation mechanisms, cambial activity, gravitropism, and the systematics and evolution of plants. After giving an outline of the variety of wood and properties of reaction wood, this review lays emphasis on various stimuli for reaction wood induction and the extensive studies carried out so far on the roles of plant hormones in reaction wood formation. Inconsistent results have been reported for the effects of plant hormones. Both auxin and ethylene regulate the formation of compression wood in gymnosperms. However, the role of ethylene may be indirect as exogenous ethylene cannot induce compression wood formation. Tension wood formation is mainly regulated by auxin and gibberellin. Interactions among hormones and other substances may play important parts in the regulation of reaction wood formation.

Control of Negative Gravitropism and Tension Wood Formation by Gibberellic Acid and Indole Acetic Acid in Fraxinus mandshurica Rupr. var. japonica Maxim Seedlings

In the present study, we Investigated the role of glbberelllc acid （GA3） and Indole acetic acid （IAA） In the gravity response of stems and tension wood formation using two-year-old stems of Fraxinus mandshurica Rupr. var. Japonica Maxim seedlings. Forty-five seedlings were used and divided Into nine groups that Included five seedlings In each group. Seedlings were treated with applications of GA3 alone at concentrations of 2.89×10^-8 and 2.89×10^-7 μmol/L, IAA alone at concentrations of 5.71×10^-8 and 5.71×10^-7 μmol/L, or their combination to the apical bud of the stem using a mlcroplpette. Seedlings were positioned horizontally after the first treatment. The same treatments were repeated six times per week. At the end of the experiment, all seedlings were harvested. Then, stem segments were cut under a light microscope. Application of exogenous GA3 at the higher concentration stimulated the upward bending of stems, whereas exogenous IAA had no effect. A synergistic effect of GA3 and IAA on upward stem bending was observed following application of the two combinations of GA3 and IAA. Moreover, application of exogenous GA3 at the higher dose stimulated wood formation on both the upper and lower sides of the stems, whereas the mixture of GA3 and IAA had a synerglstic effect on wood formation In horizontal stems. Application of exogenous IAA alone at the lower concentration （5.71×10^-8 μmol/L） or application of a mixture of the higher concentrations of GA3 （2.89×10^-7 μmol/L） and IAA （5.71×10^-7 μmol/L） Inhibited the development of gelatinous fibers （the G-layer） of tension wood on the upper side of the horizontal stems. The differentiation of gelatinous fibers of tension wood was not Inhibited by GA3 when It was applied alone, whereas the development of the gelatinous fibers of tension wood was strongly affected by the application of IAA. The findings of the present study suggest that the development of the G-layer Is not related to the dose of GA3, but needs a relatively lower concentration of IAA.

The Photomorphogenic Central Repressor COP1: Conservation and Functional Diversification during Evolution

Green plants on the earth have evolved intricate mechanisms to acclimatize to and utilize sunlight.In Arabidopsis,light signals are perceived by photoreceptors and transmitted through divergent but overlapping signaling networks to modulate plant photomorphogenic development.COP1(CONSTITUTIVE PHOTOMORPHOGENIC 1)was first cloned as a central repressor of photomorphogenesis in higher plants and has been extensively studied for over 30 years.It acts as a RING E3 ubiquitin ligase downstream of multiple photoreceptors to target key light-signaling regulators for degradation,primarily as part of large protein complexes.The mammalian counterpart of COP1 is a pluripotent regulator of tumorigenesis and metabolism.A great deal of information on COP1 has been derived from whole-genome sequencing and functional studies in lower green plants,which enables us to illustrate its evolutionary history.Here,we reviewthe current understanding about COP1,with a focus on the conservation and functional diversification of COP1 and its signaling partners in different taxonomic clades.

Molecular basis underlying rice tiller angle:Current progress and future perspectives

Crop plant architecture is an important agronomic trait that contributes greatly to crop yield.Tiller angle is one of the most critical components that determine crop plant architecture,which in turn substantially af-fects grain yield mainly owing to its large influence on plant density.Gravity is a fundamental physical force that acts on all organisms on earth.Plant organs sense gravity to control their growth orientation,including tiller angle in rice(Oryza sativa).This review summarizes recent research advances made using rice tiller angle as a research model,providing insights into domestication of rice tiller angle,genetic regulation of rice tiller angle,and shoot gravitropism.Finally,we propose that current discoveries in rice can shed light on shoot gravitropism and improvement of plant tiller/branch angle in other species,thereby contributing to agricultural production in the future.

Membrane Steroid Binding Protein 1 （MSBP1）Stimulates Tropism by Trafficking and Auxin Regulating Vesicle Redistribution

Overexpression of membrane steroid binding protein 1 （MSBP1） stimulates the root gravitropism and antigravitropism of hypocotyl, which is mainly due to the enhanced auxin redistribution in the bending regions of hypocotyls and root tips. The inhibitory effects by 1-N-naphthylphthalamic acid （NPA）, an inhibitor of polar auxin transport, are suppressed under the MSBP1 overexpression, suggesting the positive effects of MSBP1 on polar auxin transport. Interestingly, sub-cellular localization studies showed that MSBP1 is also localized in endosomes and observations of the membraneselective dye FM4-64 revealed the enhanced vesicle trafficking under MSBP1 overexpression. MSBPl-overexpressing seedlings are less sensitive to brefeldin A （BFA） treatment, whereas the vesicle trafficking was evidently reduced by suppressed MSBP1 expression. Enhanced MSBP1 does not affect the polar localization of PIN2, but stimulates the PIN2 cycling and enhances the asymmetric PIN2 redistribution under gravi-stimulation. These results suggest that MSBP1 could enhance the cycling of PIN2-containing vesicles to stimulate the auxin redistribution under gravi-stimulation, providing informative hints on interactions between auxin and steroid binding protein.

Role of GA_3,GA_4 and Uniconazole-P in Controlling Gravitropism and Tension Wood Formation in Fraxinus mandshurica Rupr. var. japonica Maxim. Seedlings

GA3 and GA4 （gibberellins） play an important role in controlling gravitropism and tension wood formation in woody angiosperms. In order to improve our understanding of the role of GA3 and GA4 on xylem cell formation and the G-layer, we studied the effect of GA3 and GA4 and uniconazole-P, which is an inhibitor of GA biosynthesis, on tension wood formation by gravity in Fraxinus mandshurica Rupr. var. japonica Maxim. seedlings. Forty seedlings were divided into two groups; one group was placed upright and the other tilted. Each group was further divided into four sub-groups subjected to the following treatments： 3.43 x 10-9 lunol acetone as control, 5.78 x 10-8 lunol gibberellic acid （GA3）, 6.21 x 10-8 lunol GA4, and 6.86 x 10-8 lunol uniconazole-P. During the experimental period, GAs-treated seedlings exhibited negative gravitropism, whereas application of uniconazole-P inhibited negative gravitropic stem bending. GA3 and GA4 promoted wood fibers that possessed a gelatinous layer on the upper side, whereas uniconazole-P inhibited wood formation but did not inhibit the differentiation of the gelatinous layer in wood fibers on the upper side. These results suggest that： （i） both the formation of gelatinous fibers and the quantity of xylem production are important for the negative gravitropism in horizontally-positioned seedlings; （ii） GA3 and GA4 affect wood production more than differentiation of the gelatinous layer in wood fibers; G-layer development may be regulated by other hormones via the indirect-role of GA3 and GA4 in horizontally-positioned F. mandshurica seedlings rather than the direct effect of GAs; and （iii） the mechanism for upward wood stem bending is different to the newly developed shoot bending in reaction to gravity in this species.

Targeted Gene Knockouts Reveal Overlapping Functions of the Five Physcomitrella patens FtsZ Isoforms in Chloroplast Division, Chloroplast Shaping, Cell Patterning, Plant Development, and Gravity Sensing

Chloroplasts and bacterial cells divide by binary fission. The key protein in this constriction division is FtsZ, a self-assembling GTPase similar to eukaryotic tubulin. In prokaryotes, FtsZ is almost always encoded by a single gene, whereas plants harbor several nuclear-encoded FtsZ homologs. In seed plants, these proteins group in two families and all are exclusively imported into plastids. In contrast, the basal land plant Physcomitrella patens, a moss, encodes a third FtsZ family with one member. This protein is dually targeted to the plastids and to the cytosol. Here, we report on the targeted gene disruption of all ftsZ genes in R patens. Subsequent analysis of single and double knockout mutants revealed a complex interaction of the different FtsZ isoforms not only in plastid division, but also in chloroplast shaping, cell patterning, plant development, and gravity sensing. These results support the concept of a plastoskeleton and its functional integration into the cytoskeleton, at least in the moss R patens.