Regulation of soybean stem growth habit: A ten-year progress report

Shang-Shang Xiong, Dan-Dan Guo, Zhao Wan, L Quan, Wn-Tian Lu,Yongguo Xu, Baohui Liu,f,*, Hong Zhai,*

a State Key Laboratory of Black Soils Conservation and Utilization,Northeast Institute of Geography and Agroecology,Chinese Academy of Sciences,Harbin 150081,Heilongjiang,China

b Key Laboratory of Soybean Molecular Design Breeding,Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, Heilongjiang, China

c College of Life Science, Northeast Agricultural University, Harbin 150030, Heilongjiang, China

d College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China

e Institute of Soybean Research, Heilongjiang Provincial Academy of Agricultural Sciences, Harbin 150086, Heilongjiang, China

f Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou 510006, Guangdong, China

Keywords:Stem growth habit Photoperiod Soybean Molecular mechanism

ABSTRACT Stem growth habit dictates plant architecture and influences flowering and podding(seed setting),making it an essential morphological and breeding agronomic trait of soybean (Glycine max).Stem growth habit in soybean is affected by photoperiod and environment and is determined by genetic variation at major genes.Classical genetic analysis identified two critical loci, designated Determinacy 1 (Dt1) and Determinacy 2 (Dt2).Dt1 is an ortholog of Arabidopsis thaliana TERMINAL FLOWER1 (TFL1) and specifies an indeterminate stem growth habit,whereas Dt2 specifies a semi-determinate growth habit.MADS-box proteins, including Dt2, SUPPRESSOR OF OVEREXPRESSION OF CO1 (GmSOC1) and MADS-box genes downregulated by E1 (GmMDE), repress Dt1 expression.Photoreceptors encoded by the E3 and E4 loci regulate the expression of soybean FLOWERING LOCUS T (GmFT) orthologs via circadian clock genes and E1,and GmFTs compete with Dt1 to regulate stem growth habit.Study of the molecular mechanism underlying the regulation of stem growth habit in soybean has focused on the repression of Dt1 expression.Here we provide an overview of progress made in elucidating the genetic and molecular bases of stem growth habit in soybean, with emphasis on the molecular components responsible for integrating photoperiodic flowering and stem growth habit.

1.Introduction

The stem growth habit of soybean (Glycine max), also called pod-bearing or stem termination type, refers to timing of the termination of apical stem growth and is a morphological breeding target [1].Stem growth habit affects many agronomic traits,including the duration of maturity,plant height,number of nodes,pod distribution,and node density,making it a determinant of soybean plant architecture and contributing to plant environmental adaptability and yield.The regulation of stem growth habit occurs in two main stages.In the first stage, shoot apical meristems(SAMs) transform into inflorescence meristems (IMs), from which floral meristems(FMs)form to produce flowers in the second stage[2–4].

In the model dicot Arabidopsis thaliana, the regulation of stem growth has been extensively studied.TERMINAL FLOWER1 (TFL1)delays the transition from vegetative growth to flowering and maintains the indeterminate growth of SAM by repressing the expression of APETALA1 (AP1) and LEAFY (LFY) [5–7].AP1 and LFY are so-called FM identity genes that induce the formation of IMs to promote flowering and inhibit stem growth in SAMs in Arabidopsis [8–12].TFL1 and its paralogs possess transcriptional repression activity but lack DNA-binding domains in their target regulatory sequences [13,14].TFL1 and related proteins form a complex with the basic leucine zipper (bZIP) transcription factor FD,which can directly bind to ACGT cis-acting elements in the promoters of target genes [8,9,15,16].FLOWERING LOCUS T (FT) protein acts as florigen to activate the expression of floral identity genes [8,9,17].TFL competes with FT for binding to FD, providing a biochemical basis for their antagonistic roles at shared FDbound target loci [18].Putative orthologs of TFL1 are widely conserved in flowering plants, in which they repress flowering.Functional orthologs of TFL1 are Dt1 in soybean [19,20], DETERMINATE(DET) in pea (Pisum sativum) [21], and PvTFL1y in common bean(Phaseolus vulgaris)[22],all of which encode proteins that suppress flowering at the shoot apex to produce an indeterminate or semideterminate stem.

Soybean,a typical short-day crop, flowers only under photoperiods shorter than a critical daylength.Photoperiod regulates not only flowering but also plant architecture, including plant height,number of nodes along the main stem,pod distribution,and number of pods per plant.These traits are all related to stem growth habit and ultimately dictate yield [23–25].Here we review recent advances in elucidating the molecular basis and regulatory mechanism of soybean stem growth habit and summarize current understanding of the molecular network underlying photoperiodic flowering and stem growth habit in this crop.

2.Classification and characteristics of soybean stem growth habit

Soybean stem growth habit has been classified into three types:indeterminacy, semi-determinacy, and determinacy [1,26].Cultivars with a determinate stem growth habit usually terminate stem growth immediately after flowering and produce a very short stem typically with a long inflorescence at the terminal node,thus forming a cluster of pods at the top.Cultivars with a determinate stem growth habit often flower and bear pods from the upper middle of the main stem and then downward.The flowering period of cultivars with a determinate stem growth habit is condensed.These cultivars have a shorter growing period, a more compact plant architecture, and higher stress tolerance [27–29].

In cultivars with an indeterminate stem growth habit, stem growth continues for several weeks after the onset of flowering,producing a tall and tapered stem with slender top internodes.The number of pods per node usually decreases near the top of the stem,such that these cultivars rarely produce more than three pods at the terminal node[20].Cultivars with indeterminate stems typically flower and form pods starting from the bottom of the main stem and continuing upward as growth continues.Indeterminate cultivars flower for a much longer period than do determinate cultivars [20].They are often barrenness-resistant [20,27–29].

Semi-determinate cultivars are intermediate between indeterminate and determinate cultivars [1].In these cultivars, the stem tip continues vegetative growth after a period of flowering,but this happens earlier than in indeterminate cultivars, resulting in fewer nodes on the main stem than in indeterminate cultivars.However,semi-determinate cultivars produce stems with terminal racemes as do determinate cultivars; they also produce a long, tapering stem that is distinctly thicker at the tip than that of indeterminate cultivars.Semi-determinate cultivars usually bear flowers and pods from the bottom of the main stem and then upward to the tip, as do indeterminate cultivars [1,28,29].Cultivars with a semi-determinate stem growth habit have more flowers and pods,often yielding more grain in irrigated production systems with sufficient water and fertilization than indeterminate cultivars[1,30,31].

The stem growth habit of soybean is regulated mainly by genetic factors,but is also influenced by ecological conditions such as photoperiod, shading, and lodging.The latter two conditions cause a semi-determinate stem to adopt a more indeterminate appearance.Long-day photoperiods can induce the switch from a determinate to a semi-determinate stem [1,32].

The classification of soybean cultivars into one of the three types of stem growth habit is robust in some but not all environments,as some growth conditions result in indistinguishable stem growth phenotypes [1,26].The duration of the overlap between vegetative and reproductive growth is at the core of the classification in soybean [1].Determinate stems undergo clearly separated stages of vegetative and reproductive growth.By contrast,indeterminate stems present more overlap between the vegetative and reproductive states, resulting in better adaptation to the shorter growing season in the north of China [33].Most soybean cultivars grown in northern China have an indeterminate habit,with a gradual increase in the proportion of determinate soybean cultivars from north to south China[19].Vegetative and reproductive organs compete for photosynthetic products when the two periods overlap [33].In general, high-yielding cultivars are characterized by a short overlap between vegetative and reproductive periods that limits the competition for photosynthetic assimilates between vegetative and reproductive organs and facilitates the development of pods and seeds [19,33].Thus, stem growth habit of soybean is a trait that is closely related to the reproductive period of soybean.

3.Identification of classical loci that control stem growth habit

Classical genetic analysis showed[1]that stem growth habit in soybean is modulated primarily by Dt1 and Dt2.Dt1 confers an indeterminate stem growth habit [1], while Dt2 confers a semideterminate growth habit[34].Dt1 is incompletely dominant over dt1, as plants heterozygous for Dt1 (Dt1/dt1) exhibit a semideterminate phenotype, while Dt2 is fully dominant over dt2, as both plants homozygous for Dt2(Dt2/Dt2)and plants heterozygous for Dt2(Dt2/dt2)display a semi-determinate phenotype.Dt1 exerts an epistatic effect on Dt2 [1,19,20,34–36].In plants homozygous for Dt1, the Dt2 genotype (Dt2/dt2 or Dt2/Dt2) induces a semideterminate growth habit,while plants homozygous for the recessive dt2 allele present an indeterminate growth habit [19–22,34].Finally,plants homozygous for the dt1 allele produce only determinate stems, regardless of the genotype at Dt2 [19,20,34–36].

Woodworth [37] was the first to propose that the allele at Dt1 controlled stem growth habit.The segregation ratio between plants with a determinate stem growth habit and those with indeterminate growth was 3:1 in an F2mapping population,indicative of a single locus.Many years later,Liu et al.[38]identified a single major quantitative-trait locus (QTL) for determinate growth habit that was mapped to a region flanked by markers Sat_099 and Satt006 on linkage group L overlapping with the genetic location of Dt1.With the sequencing of the soybean genome, Schmutz et al.[39] renamed linkage group L as chromosome 19 (Gm19).Using a candidate-gene approach, Dt1 was cloned and characterized by two research groups [19,38].Dt1 was shown to be Glyma19g37890, an ortholog of Arabidopsis TFL1 named GmTFL1b.An analysis[19]of natural variation at GmTFL1b in wild and cultivated soybean populations identified four functional single-nucleotide polymorphisms (SNPs) in Dt1, designated dt1-ab, dt1-ta, dt1-bb and dt1-tb, resulting in four distinct amino acid substitutions in the predicted corresponding dt1 proteins.Each variant was associated with a phenotypic change from indeterminate to determinate stem growth habit.

The Dt2 locus was mapped to the classical linkage group LG#6[40] and further assigned to linkage group LG G [41], based on SSR markers.With the soybean genome sequenced, Dt2 was mapped to the end of the short arm of chromosome 18, based on the genomic location of its linked gene, isozyme mannose-6-phosphate isomerase (MPI) [39,40].Using a mapping population derived from a cross between the cultivars NE3001 (Dt2/Dt2 Dt1/Dt1) and ‘IA3023′(dt2/dt2 Dt1/Dt1) [30], Dt2 was mapped to a genomic region between markers SSR_18_1821 and SSR_18_1825, spanning 81 kb and containing 10 predicted genes[34].A sequence comparison between semi-determinate and indeterminate cultivated soybean accessions and G.soja facilitated the identification of Glyma18g50910 as the best candidate for Dt2[34],with 37 SNPs distinguishing determinate from indeterminate accessions.These 37 SNPs are distributed in the noncoding sequence or flanking regulatory elements of Glyma18g50910,rather than in the coding region, causing differential expression of Dt2 as a function of the allele[34].Dt2 determines stem branching in soybean,with two SNPs located in its promoter region being responsible for significant differential transcript levels between two major haplotypes [42].The same two SNPs may also be involved in determining stem growth habit.

4.The major genes of soybean controlling stem growth habit

4.1.Dt1 and its homologs

Dt1 (GmTFL1b), the functional ortholog of TFL1 in Arabidopsis,encodes phosphatidylethanolamine-binding proteins and represses flowering[19,20,43].Dt1 is expressed primarily in SAMs to suppress terminal flowering and promote shoot apical growth during the vegetative phase in soybean [19,20].Dt1 suppresses the floral transition of the SAM by repressing the expression of FM identity genes, GmAP1 and GmLFY [44].The transition of the SAM from vegetative to reproductive growth depends on Dt1 transcript abundance [20,24].Dt1 expression in determinate soybean cultivars decreases rapidly after flowering but remains high for some time in indeterminate soybean cultivars during the postflowering stage [20].Studies of the molecular regulatory pathway behind soybean stem growth habit have concentrated largely on how Dt1 expression is modulated.

Dt1 has three paralogs in soybean: GmTFL1a, GmTFL1c and GmTFL1d[20,45].These four related genes form two homoeologous pairs,GmTFL1a with Dt1 and GmTFL1c with GmTFL1d,both derived from an ancient whole-genome duplication event.GmTFL1c and GmTFL1d are highly expressed in the shoot apex, with lower expression in leaves and flowers[45].By contrast,Dt1 is expressed only in roots and at the tip of the stem[20].The tfl1c/tfl1d double mutant exhibited accelerated flowering time [45].GmTFL1c and GmTFL1d interact with the bZIP transcription factor FDc1 in the SAM to repress the expression of the FM identity gene GmAP1a[20,45].

4.2.Dt2

Dt2, an ortholog of APETALA1/SQUAMOSA (AP1/SQUA) from Arabidopsis, encodes a MADS-box transcription factor that binds directly to the CArG-box motif in the promoter of downstream genes to regulate their transcription [34,46].Dt2 possesses a Keratin-box (K-box) structural domain; most proteins with such domains can form homodimers or heterodimers [47–50].As a MADS-domain factor with a presumed role in transcription, Dt2 localizes to the nucleus[36].Dt2 directly binds to the first,second,and fifth CArG-box motifs in the Dt1 promoter region to repress its transcription, thus promoting early conversion of the SAMs into FMs[35,36,44].Dt2 encoded by the dominant Dt2 allele suppresses Dt1 expression, leading to a semi-determinate phenotype [36,44].The loss of Dt2 function alleviates the suppression of Dt1 expression and leads to high Dt1 transcript levels,resulting in an indeterminate phenotype [34–36,44].Soybean cultivars carrying the Dt2/Dt2 Dt1/Dt1 genotype show a semi-determinate stem growth habit and those carrying the dt2/dt2 Dt1/Dt1 genotype show an indeterminate stem growth habit [1,19,20,34–36].

4.3.SOC1a (GmSOC1) and SOC1b

Soybean SOC1a (also called GmSOC1) is a putative ortholog of Arabidopsis SOC1, encoding another MADS-domain transcription factor.SOC1a binds to the fifth CArG-box motif in the Dt1 promoter to repress its transcription.Both Dt2 and SOC1a are essential for the transcriptional repression of Dt1, although the repression of Dt1 exerted by SOC1a is weaker than that exerted by Dt2 [35,51].SOC1a is partner of Dt2 in regulating stem growth habit, with interactions at the transcriptional and protein levels [35].Dt2 directly interacts with SOC1a through their K-domains, and Dt2 induces SOC1a expression.Heterologous expression of Dt2 fails to repress TFL1 transcription in Arabidopsis in the absence of SOC1,indicating that the cooperation of Dt2 and SOC1 is essential for the repression of Dt1 transcription.In soybean, proper spatiotemporal co-expression of Dt2 and SOC1a is essential for the establishment of semi-determinacy [35].

Kou et al.[51] reporte that SOC1b, the duplicated paralog of SOC1a,also regulates flowering and stem node number in soybean.The protein sequences of SOC1b and SOC1a are 97.2%identical,differing by only six amino acids.The soc1a and soc1b single mutants and the soc1a soc1b double mutant all exhibit delayed flowering and maturation,with more nodes along the main stem and higher grain weight per plant under both long-day (LD) and short-day(SD) conditions.The phenotype exhibited by the soc1a soc1b double mutant is stronger than that of either single mutant, and the soc1a single mutant displays a more pronounced phenotype than does the soc1b single mutant.This phenotypic variation between SOC1a and SOC1b is a reflection of the higher transcriptional level of SOC1a than of SOC1b.SOC1b also interacts with Dt2 to repress Dt1 expression but does not bind to the Dt1 promoter directly,acting instead as a cofactor for the SOC1a-Dt2 complex to transcriptionally repress Dt1 [51].SOC1a and SOC1b can form homodimers or heterodimers,the activity of the latter being hypothesized to be greater than that of their respective homodimers [51].SOC1a and SOC1b can also bind to the CArG-box motifs present in the promoters of GmFT5a and GmFT2a in leaves to increase their transcription and promote floral transition [34,35,44,46,51].

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4.4.GmFTs

In Arabidopsis, FT competes with TFL1 for binding to FD to induce the expression of FM identity genes, AP1 and LFY [17].In soybean, GmFT2a and GmFT5a function in floral induction [52],but GmFT5a is markedly more effective than GmFT2a for stem determinacy control [44,53].GmFT5a promotes floral transition at the SAM by competing with Dt1 for binding to FDc1 to regulate the transcription of the FM identity genes GmAP1a, GmAP1b and GmAP1c [44,53].GmFT5a, but not GmFT2a, interacts with FDc1[44].The differing combinations of protein–protein interaction between these factors may help explain the differing roles of GmFT2a and GmFT5a in controlling stem determinacy [44,52,53].GmFT5a acts independently of the Dt2 genotype to terminate stem growth, given that overexpression of GmFT5a resulted in almost the same stem determinacy phenotype in the dt2 and Dt2 genetic backgrounds [44,53].

FT also acts as a flowering repressor.Antagonistic roles in flowering-time regulation have been postulated for FT-like proteins in several plant species [54–63].Overexpression of GmFT1a in soybean delays flowering and maturation, producing more nodes along the main stem and taller plants, with a much longer period of vegetative growth after initiation of flowering [54].This observation suggests that GmFT1a controls stem determinacy.GmFT1a down-regulates the expression of the floral organ identity specification genes, including GmAP1b and GmAP1c.

4.5.GmAP1s

AP1,encoding another MADS-box transcription factor,functions as a class A gene in the ABCDE model for determining flower meristems as well as petal and sepal differentiation in Arabidopsis [11].GmAP1s are orthologs of Arabidopsis AP1 [53,64].Four GmAP1

homologs: GmAP1a, GmAP1b, GmAP1c, and GmAP1d, are present in the soybean genome [64,65].The gmap1 quadruple mutant is late-flowering and produces more nodes and taller plants,whereas overexpression of GmAP1a results in early-flowering and morecompact plants [65].

GmAP1s act downstream of GmFTs and Dt1.GmFT5a interact with FD-LIKE 06 (GmFDL06) and GmFDc1.GmFDc1 is primarily expressed in the early vegetative growth phase to promote the floral transition and initiate floral development in SAMs.The GmFTGmFD complex directly induces GmAP1 transcription to promote terminal flowering[44,53].Dt1 competes with GmFT5a for binding to GmFDc1,with the Dt1-GmFDc1 complex binding directly to the ACGT cis-element in the GmAP1s promoter to suppress its transcription[44,53].The Dt1-GmFDc1 complex maintains the vegetative growth of soybean SAMs[44,53].GmAP1s bind directly to the Dt1 promoter for transcriptional repression, whereby Dt1 and GmAP1s form a suppressive regulatory feedback loop [44,52,53].When Dt1 is highly expressed in vegetative SAMs, expression of GmAP1s is also repressed at the same site to help maintain shoot indeterminacy[44,53].When Dt1 is absent or Dt1 transcript levels are downregulated, GmAP1s are expressed in the shoot apices and convert SAMs to FMs[44,52,53].This suppressive regulatory feedback loop between Dt1 and GmAP1s helps maintain a balance between flower development and shoot indeterminacy [44,53].

5.Integration of photoperiodic flowering and stem growth habit

Soybean plants exhibit different stem growth habits when grown under LD and SD conditions [24].E1 exerts the greatest effect on photoperiod sensitivity[66–69] and is the core regulator of soybean photoperiodic responses[66–69].E1 was cloned using a map-based approach and shown to function as a flowering repressor [67].E1 is a legume-specific gene.Genome editing of E1 via clustered regularly interspaced short palindromic repeat(CRISPR)/CRISPR-associated nuclease 9(Cas9)revealed its involvement in determining stem growth habit [70].The wild-type cultivar Tianlong 1, carrying the dominant and functional E1 allele,presents an indeterminate stem growth habit under LD conditions but switches to a determinate stem growth under natural SD conditions[67,70].By contrast,e1 mutants exhibit a determinate stem growth habit regardless of photoperiod [70].Dt1 expression is downregulated while that of Dt2 is upregulated in e1 mutants[70].Expression of a set of MADS-box genes is upregulated in the shoot apex of e1 mutants, suggesting a role for E1 in photoperiod-regulated stem growth habit [70].

GmMDE are MADS-box transcription factors with a K-box structural domain that act directly downstream of E1[71].E1 mediates the epigenetic silencing of GmMDE transcription by directly binding to their promoters and increasing levels of trimethylation of lysine 27 on histone H3 (H3K27me3) [71].GmMDE and GmFT2a/GmFT5a form a positive regulatory feedback loop for signal amplification, thus promoting flowering [71].GmMDE06 promotes the termination of apical stem growth by repressing Dt1 transcription[71].The E1-GmMDE-GmFT2a/5a-Dt1 signaling pathway forms the basis of the molecular mechanism behind photoperiod-regulated stem growth habit [71].

E3 and E4 are homologs of the photoreceptor phytochrome A[72,73],which is critical to adequately sensing photoperiod signals and transmitting them to modulate the expression of downstream genes.E3 and E4 induce and maintain Dt1 expression under LD conditions [24].Cultivars carrying functional alleles at E3 or E4 exhibit photoperiod-regulated changes in stem growth habit[24].The mechanism by which E3 and E4 affect stem growth habit is now well understood.They are involved in the photoperiodic control of E1 at both the transcriptional and posttranscriptional levels via circadian clock genes[74–77].E3 and E4 directly interact with LUX ARHTYHMO (LUX) to mediate its degradation, which alleviates the LUX-dependent repression of E1 transcription [78].E3 and E4 also directly interact with and stabilize E1 [78].They negatively regulate the expression of J, the ortholog of Arabidopsis EARLY FLOWERING 3 (ELF3), whose encoded protein physically binds to the E1 promoter to downregulate its transcription.They positively regulate the expression of Time of flowering 11 (Tof11)and Tof12, encoding orthologs of the Arabidopsis circadian clock protein PSEUDORESPONSE-REGULATOR 3 (PRR3), which acts via LATE ELONGATED HYPOCOTYL (LHY) to promote E1 expression[76].J, PRR3, LUX, and LHY are all circadian clock genes.E3 and E4 regulate E1 expression via these genes and thus their downstream targets GmFTs, including GmFT2a, GmFT5a, and GmFT1a[52,67,71,79–81].GmFTs directly regulate the expression of the floral organ identity genes or compete with Dt1,ultimately regulating stem growth habit of soybean [17,44,52,53].

6.Conclusions and perspectives

Fig.1.A model summarizing the regulation mechanism of soybean stem growth habit under long-day and short-day conditions.Solid arrows indicate activation.‘‘T”represents repression.Dotted arrows indicate the movement direction of proteins.Gray arrows represent a decline in strength.

Great progress has been made in the study of soybean stem growth habit using physiological, genetic, and molecular biology tools.We now have a clear understanding of the molecular basis and regulatory pathway that control stem growth habit in soybean.The Dt1–Dt2 module is the core regulator of stem growth (Fig.1).Determinacy and indeterminacy represent two extremes of stem growth habit.Loss of Dt1 function is associated with a determinate stem growth habit, in contrast to the indeterminate stem growth habit expressed when Dt1 is functional.Between these two extremes, a moderate repression of Dt1 expression by Dt2 results in soybean plants with a semi-determinate stem growth habit.In short, the stem growth habit of soybean is a reflection of Dt1 expression levels.

Besides Dt2,the proteins SOC1a,GmFT5a,GmFT1a,GmAP1,and GmMDE06 are involved in the regulation of Dt1.Dt2, SOC1a,SOC1b, and GmAP1s all belong to the MADS-box family of transcription factors with K-box structural domains[34,35,44,46].Such proteins can form homo- or heterodimers.It will be desirable to learn how these proteins interact to finely and synergistically regulate soybean stem growth habit.Soybean cultivars with the same stem growth habit, especially with a semi-determinate growth habit, exhibit differences in related traits such as the number of main stem nodes.Pods growing from these nodes increase soybean yield.The fine-modulation mechanism of Dt1 remains to be deciphered.Identification of additional genes that participate in these pathways and their modes of regulation is needed to improve adaptation and grain yield in soybean via molecular design breeding.

Breeding for higher yield and earlier maturity is a major goal of soybean agriculture, particularly in the northeast region of China,which experiences shorter, permissive growth conditions.The major soybean-producing areas in China have started to undergo a gradual shift northward, where the growing season is shorter than at more southern latitudes.For plants to reach maturity and produce high yields during this shorter growing season, ultraearly-maturing soybean cultivars are needed.Given that stem growth and flowering are regulated by photoperiod and photoperiod-related genes,early flowering is often associated with early termination of apical stem, producing short plants with low grain yields and limiting further yield improvement.In the future,with a better understanding of the molecular mechanism and regulatory network of photoperiod and stem growth habit, it may be possible to manipulate photoperiod and stem growth habit-related genes simultaneously using high-efficiency breeding approaches,breaking the association between the photoperiod and the stem growth habit pathways and ultimately resolving the current tradeoff between early maturity and high yield.

CRediT authorship contribution statement

Shangshang Xiong:Formal analysis, Visualization, Writing -original draft.Dandan Guo:Writing – review & editing.Zhao Wan:Writing – review & editing.Le Quan:Writing – review &editing.Wen-Tian Lu:Writing – review & editing.Yongguo Xue:Writing–review&editing.Baohui Liu:Writing–review&editing.Hong Zhai:Writing – original draft, Writing – review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We thank Xi Li for writing assistance and Xiaobin Zhu and Libing Dong for proofreading the manuscript.This work was supported by the National Key Research and Development Program of China(2021YFD1201101),the National Natural Science Foundation of China(32272187),Young Scientists Group Project of Northeast Institute of Geography and Agroecology (2022QNXZ05), and Natural Science Foundation of Heilongjiang Province of China(YQ2021C034).