Multidimensional molecular strategies for crop photoperiod adaptation and latitudinal expansion-

1 Introduction

The continued expansion of the global population, together with the rising frequency of extreme weather events, has placed considerable pressure on efforts to ensure food security and maintain a stable supply of essential agricultural products (Godfray et al., 2010). During natural evolution and early artificial domestication, crops acquired strong adaptability to the climatic conditions prevailing in their regions of origin (Meyer and Purugganan, 2013). However, as arable land resources become increasingly scarce, the introduction and expansion of crops from their original habitats into other latitudinal zones have become an unavoidable trend in modern agricultural development. During crop range expansion, environmental factors such as photoperiod, which regulate flowering time, function as major constraints (Jung and Müller, 2009; Nakamichi, 2015). When crops are introduced into new latitudes, changes in external light signals can induce abnormal flowering (e.g., delayed or premature onset) and restrict biomass accumulation, ultimately resulting in substantial yield losses. Therefore, overcoming inherent photoperiod constraints and improving environmental adaptability are essential for successful cross-regional introduction and expansion, as well as for increasing crop yields.

The latitudinal expansion of crops represents more than a geographical shift; it is a complex evolutionary process involving coordinated reprogramming across genomic, epigenomic and transcriptomic layers (Hufford et al., 2012; Liu et al., 2020). However, a unified theoretical framework connecting multi-scale evolutionary drivers with contemporary molecular strategies remains notably lacking. Consequently, research in this field remains fragmented across individual scales or isolated trait modifications and does not fully address the integrated breeding objectives required for pyramiding cross-latitude adaptive traits. Accordingly, we examine the multidimensional adaptive strategies that underlie range expansion, including population-level point mutations, epigenetic modifications, structural variations, and copy number variations. Furthermore, we discuss the challenges associated with reshaping future agricultural landscapes from the perspectives of multi-level genetic information reprogramming and the coordinated optimization of adaptive expansion while retaining superior traits.

2 Tracing the discovery and breeding trajectories of photoperiodism in crops

Crops geographic distribution and adaptive range expansion are closely tied to photoperiodic responses. Scientific inquiry into this phenomenon dates back to the early 20th century, when W. W. Garner and H. A. Allard discovered that tobacco flowering is regulated by seasonal day length. They observed that while tobacco plants remained vegetative in summer, they flowered normally in winter greenhouses. Intriguingly, artificially shortening the daytime length in summer accelerated flowering, whereas extending winter photoperiods inhibited it. This physiological mechanism, by which plants perceive external light cues to anticipate seasonal transitions and adjust their development accordingly, came to be known as photoperiodism. Based on their responses to day length, plants are generally classified into three categories: short-day, long-day, and day-neutral plants (Amasino, 2013; Garner and Allard, 1920) (Figure 1).

Subsequent studies identified leaves as the primary organs responsible for perceiving photoperiodic signals, leading to the proposal of a mobile floral stimulus termed “florigen”, which moves through vascular tissues to the shoot apex to induce flowering (Chailakhyan, 1937). With the rapid progress of molecular biology and genetics, research on crop photoperiodism has transitioned from macroscopic observations to in-depth mechanistic exploration at the molecular level. In 2007, the FT protein was finally confirmed as the elusive florigen. Under inductive photoperiods, FT is expressed in leaf phloem companion cells, and the synthesized FT protein is then transported through the phloem to the shoot apical meristem, where it assembles florigen activation complex (FAC) with FD and 14-3-3 proteins, ultimately triggering the floral transition (Corbesier et al., 2007; Gao et al., 2026, 2025; Zhao et al., 2026) (Figure 1).

Recent advances in population genetics have made it possible to trace crop evolutionary trajectories during domestication and range expansion. Leveraging advanced approaches such as genome-wide association studies (GWAS) and gene recombination technologies, key regulatory genes governing photoperiodic responses in crops have been identified, along with critical natural variants and point mutations that lead to loss-of-function or enhanced/weakened activity of these genes. These genetic alterations have modified the intrinsic photoperiod sensitivity of crops, thereby effectively removing the geographical constraints that once limited their transregional expansion. As a result, large-scale introduction and substantial yield enhancement have been achieved worldwide—a trend particularly notable in cotton, which has undergone a remarkable transition from a photoperiod-sensitive wild type to a day-neutral cultivated form (Andrés and Coupland, 2012).

3 Multidimensional molecular evolutionary dynamics in reshaping crop photoperiod adaptation

The adaptation of crops to photoperiods and their global expansion across different regions are not dependent on a single genetic strategy. Rather, they are associated with a multidimensional synergistic approach involving genomic structural variations (including population-level point mutations and large-scale genomic variations) as well as epigenetic modifications. Ultimately, these mechanisms break the original photoperiod constraints by reshaping the floral induction signaling pathways, thereby enabling crops to better adapt to diverse ecological environments across different latitudes worldwide (Figures 2; Table 1).

Table 1. Functional roles of environmental adaptation-related factors in crops.

3.1 Reshaping photoperiod adaptation at the population point mutation level

Haplotypes derived from widespread single nucleotide polymorphisms (SNPs) serve as key genetic strategies for regulating flowering time and adapting to diverse latitudinal environments. GWAS have identified several superior haplotypes facilitating soybean latitudinal expansion, such as SOC1a, GmSGF14^H4, and GmSTOP1a. Among these, a critical A/G single nucleotide polymorphism in the promoter region of Tof18 (encoding SOC1a) is associated with the divergence of natural populations into distinct haplotypes with varying transcriptional activities and significant differences in flowering time. Specifically, the haplotype carrying the Tof18G allele confers an early-flowering phenotype, significantly enhancing soybean adaptability to high-latitude environments. Conversely, the Tof18A allele results in a late-flowering phenotype, which is advantageous for adaptation in low-latitude regions (Kou et al., 2022). Additionally, a frameshift mutation in the GmSGF14^H haplotype disrupts its core 14-3–3 structural domain, resulting in a late-flowering phenotype that enhances soybean adaptability to specific latitudes (Jiang et al., 2023). Similarly, SNP analysis in cultivated rice revealed that key mutations in the OsCCA1 coding region produce haplotypes (OsCCA1a and OsCCA1d) contributing to geographic adaptation. The japonica OsCCA1a haplotype promotes flowering, enabling expansion to higher latitudes, whereas the indica OsCCA1d haplotype delays flowering to ensure stable yields in low-latitude regions. This allelic variation in flowering time regulation represents a core strategy enabling major crops to adapt across a broad range of latitudes (Lee et al., 2022). Taken together, these findings underscore that point mutations have been identified across diverse species to mediate multidimensional crop expansion. Nevertheless, these loci have been predominantly characterized in a few model crops like soybean. Consequently, the functional conservation of these genes in other major species, such as cotton, rice, and wheat, warrants further investigation.

Population-level point mutations can also lead to the functional remodeling of key flowering integrator proteins. For instance, the photoperiod-insensitive soybean cultivar K3 harbors three quantitative trait loci (QTLs) associated with late flowering. Among them, a non-synonymous mutation in the fourth exon of FT2a suppresses its repressor function, resulting in the late-flowering phenotype of K3 under long-day and high-temperature conditions (Sun et al., 2019). Similarly, in cotton, a non-synonymous mutation was identified in the coding region of GhTOFD06, which is significantly associated with delayed flowering. Further analysis revealed that the homozygous wild-type C/C genotype underwent positive selection in cultivated populations. This allele attenuates the negative regulatory effect of GhTOFD06 on flowering, thereby reducing photoperiod sensitivity and promoting early maturity (Xu et al., 2026). Collectively, these findings underscore that population-level point mutations provide a potential genetic basis for the adaptive evolution of flowering time in crops, enabling their accommodation to diverse regional environments. Despite these advances, population-level analyses of point mutations in cotton have been largely skewed towards fiber development and disease resistance, leaving the genetic basis of photoperiod adaptation poorly understood. Overall, these discoveries highlight point mutations as a pivotal genetic foundation for the adaptive evolution of flowering time, allowing crops to thrive in diverse agro-ecological zones. Future efforts to elucidate the functional conservation and divergence of loci driving latitudinal expansion across species will deepen our mechanistic understanding of photoperiodic adaptation and offer novel targets for accelerating crop expansion into new latitudes.

Notably, even when point mutations and sequence polymorphisms occur in non-coding regions, they can modulate crop traits by altering transcriptional activity. For example, a flowering time QTL on soybean chromosome 16 was identified as FT5a. The early-flowering (ef) and late-flowering (lf) alleles of this gene share identical coding sequences but harbor 15 DNA polymorphisms in the promoter, introns, and 3’UTR. These non-coding variations lead to significant differences in transcript abundance. Consequently, soybeans carrying this rare early-flowering haplotype can independently promote flowering without being regulated by the E1 gene, providing a potentialgenetic basis for early-flowering adaptation in high-latitude regions (Takeshima et al., 2016).

3.2 Reshaping photoperiod adaptation at the level of chromatin modification

Beyond structural variations in DNA sequences, crops also employ epigenetic strategies, including DNA methylation and specific histone modifications, to precisely respond to photoperiod changes (Guarino et al., 2022; Shi et al., 2023). For instance, under optimal photoperiod conditions, the methylation level at CHH sites in the genome of short-day plants like rice is significantly suppressed, thereby activating the transcription of downstream key flowering genes (Wu et al., 2024). Furthermore, the rice methyl-CpG-binding domain protein OsMBD707 alters photoperiod sensitivity and flowering time by transcriptionally regulating flowering-related genes in the Ehd1-Hd3a/RFT1 pathway (Qu et al., 2021). In cotton, a comparative analysis between Gossypium hirsutum (upland cotton) and wild cotton identified 519 differentially methylated genes (Song et al., 2017). Specifically, the COL2D gene is hypermethylated and silenced in wild cotton, conferring photoperiod sensitivity that prevents flowering during long-day summers. Conversely, demethylation-induced COL2D overexpression in domesticated cotton confers photoperiod insensitivity, potentially broadening its cultivation latitude and environmental resilience. These findings highlight the potential of epigenetic breeding in polyploidy. Furthermore, recent studies indicate that in early-maturing cotton varieties, DNA hypomethylation and elevated H3K9ac levels mediate the high expression of GhAP1 compared to late-maturing varieties (Wang et al., 2023). Whether such differential methylation-driven changes in flowering time serve as key targets for the latitudinal expansion of cotton warrants further investigation.

Histone methylation-mediated transcriptional silencing also serves as a key driver of plant adaptation to complex environments. In soybean, the transcriptional repressor E1 directly binds to the promoter region of GmMDE and specifically elevates H3K27me3 levels at this locus. This epigenetically suppresses GmMDE expression, effectively blocking the positive feedback induction of downstream GmFT2a/5a and thereby precisely coordinating flowering time (Zhai et al., 2022). In rice, the abscisic acid (ABA)-responsive kinase SAPK8 directly phosphorylates the transcription factor ABF1; upon activation, ABF1 interacts with FIE2 to recruit the PRC2 complex to the target regions of the floral activators Ehd1 and Ehd2. This markedly increases H3K27me3 deposition at these loci and represses their del transcription, ultimately aying flowering. These findings highlight a synergistic regulatory mechanism between hormone signaling and epigenetic modifications in plants (Tang et al., 2024). It will be an intriguing research direction to investigate whether differential methylation of these flowering genes mediates varietal adaptation across multiple varieties.

Notably, the epigenetic strategies adopted by crops during latitudinal adaptive expansion also extend to post-transcriptional RNA modifications. For instance, significant differences in N6-methyladenosine (m6A) modification levels have been observed between photoperiod-sensitive wild cotton and insensitive cultivated varieties, with wild types exhibiting significantly higher m6A levels under long-day conditions. Furthermore, silencing the m⁶A demethylase gene GhALKBH5 reduces the mRNA abundance of multiple key flowering genes and causes delayed flowering, suggesting that dynamic m⁶A modification and demethylation of flowering-related transcripts may directly regulate photoperiod sensitivity in cotton (He et al., 2024). However, RNA modification-mediated differences in flowering have been confirmed in only a few species, and whether they drive crop expansion across different dimensions remains unknown. In summary, through a multilayered epigenetic regulatory network encompassing DNA methylation, histone methylation, and post-transcriptional RNA methylation (m⁶A), crops can adapt to complex photoperiod conditions across different latitudes without altering the underlying genomic sequence, thereby greatly facilitating their trans-regional geographical expansion. However, it is crucial to distinguish stable, heritable epigenetic variation from transient, environmentally induced epigenetic changes. In particular, epigenetic modifications that are developmental stage-specific or environmentally driven still require more rigorous functional validation across multiple generations and fluctuating environments to establish their causal role in latitudinal adaptation.

3.3 Evolutionary trajectories of photoperiodic adaptation driven by structural variations and copy number variation

Facing extreme long-day conditions at high latitudes or short-day environments at low latitudes, conventional point mutations often fail to rapidly disrupt the established photoperiodic balance. In such cases, genomic structural variations (SVs, including large deletions and transposon mobilization) and copy number variations (CNVs) often rapidly boost crop adaptation. Distinct from single nucleotide polymorphisms (SNPs), these large-scale variations can profoundly alter gene dosage, disrupt cis-regulatory elements to rewire gene expression networks, or modify local chromatin architecture. For example, naturally occurring CNVs can directly elevate the transcriptional abundance of flowering integrators via dosage effects, while transposon insertions often disrupt repressor binding sites, thereby rapidly rewiring the flowering regulatory network.

Structural variations (SVs) causing aberrant expression or inactivation of core flowering genes are frequently observed in crop evolution. For instance, the domestication and expansion from low-latitude to high-latitude regions involved the disruption of the photoperiod-sensitive flowering repressor ZmCCT10 through a transposon insertion in its promoter region. This structural disruption reduced the photoperiod sensitivity, enabling flowering under long-day conditions and thereby accelerating its northward range expansion (Li et al., 2023). Similarly, in soybean, a Ty1-Copia-like retrotransposon (SORE-1) insertion within an intron of the FT2a gene confers allele-specific transcriptional repression, significantly reducing transcript abundance and consequently delaying flowering. This structural variant may facilitate soybean to maintain a prolonged vegetative growth phase under the short-day conditions at lower latitudes, thereby providing a genetic foundation for the further expansion of cultivation into even lower-latitude regions (Zhao et al., 2016).

Recent studies have identified a 24-bp InDel variant in the promoter of GmSTOP1a as a major genetic factor associated with soybean adaptation to acidic, low-phosphorus soils at low latitudes. Specifically, the haplotype carrying the 24-bp insertion is predominantly distributed in high-latitude soybean germplasm. This insertion disrupts the binding site for the transcription factor GmAGL12 on the GmSTOP1a promoter, thereby attenuating GmAGL12-mediated transcriptional activation of GmSTOP1a. In contrast, the 24-bp deletion allele that prevails in low-latitude soybean varieties maintains effective GmAGL12-mediated activation of GmSTOP1a, which in turn regulates the expression of multiple downstream genes involved in low-phosphorus tolerance, thus enhancing soybean fitness in acidic, phosphorus-deficient soils at low latitudes (Guo et al., 2026). Additionally, a 2089-bp deletion in the upstream promoter region of the wheat Ppd-D1a allele abolished photoperiod sensitivity and accelerated flowering under long-day conditions, thereby facilitating the widespread introduction of wheat into high-latitude regions (Beales et al., 2007).

Large-scale chromosomal structural variations (such as translocations or inversions) and cross-species large-fragment introgression are also core drivers in reshaping crop photoperiod sensitivity. Pan-genome analyses of upland cotton revealed a reciprocal translocation between A03 and A09 that delayed flowering in wild germplasm, while five large inversions (A06, A10, A12, A13, D03) broke photoperiodic constraints, conferring an extremely early-maturing phenotype. These structural variations provided the potential genetic basis for upland cotton’s expansion across diverse latitudes (Yang et al., 2026). In addition, approximately 18.16% of the upland cotton genome was introgressed from sea island cotton during domestication. This genome-wide segmental replacement enriched genetic diversity and introduced key early-maturing and high-latitude adaptive alleles, including the core photoperiod regulator GhTOFD06. This significantly advanced flowering time, thereby accelerating its global adaptation to high-latitude regions (Xu et al., 2026).

Gene copy number variation (CNV) has also played an indispensable role in the global expansion of polyploidy crops. Genetic analyses have demonstrated that multiple core genes regulating photoperiod response and vernalization requirements in the wheat genome, specifically Ppd-B1 and Vrn-A1, have undergone significant copy number amplification and differentiation. For instance, alleles carrying increased Ppd-B1 copy numbers have arisen independently at least twice during evolution, conferring a day-neutral phenotype that facilitated the introduction of wheat into diverse photoperiod environments. Concurrently, amplification of Vrn-A1 copy number strengthens the vernalization requirement, further contributing to the adaptation of wheat to overwintering conditions across different latitudes (Díaz et al., 2012; Zikhali et al., 2017). In summary, the evolutionary expansion of crops across diverse global regions has not relied on a single genetic strategy. Instead, it has been driven by a multidimensional, synergistic regulatory network that integrates population-level point mutations, epigenetic modifications, and large-scale genomic variations. These genetic adaptive strategies not only enabled crops to overcome their original geographical and climatic constraints, thereby promoting their extensive worldwide cultivation, but also furnished a rich reservoir of natural genetic variation for early human agricultural domestication.

4 Discussion

Although substantial progress has been made in understanding photoperiod-driven crop adaptive evolution, crop expansion across natural environments is governed by a highly complex combination of environmental cues. To date, studies of crop adaptive evolution have concentrated mainly on the single dimension of photoperiodic signaling (González-Delgado et al., 2025). However, photoperiod is not the sole determinant of latitudinal adaptation; rather, it involves intricate genotype-by-environment (G×E) interactions with temperature, water availability, precipitation, and soil conditions (George et al., 2024; Jung et al., 2023). For instance, under specific high-latitude photoperiod regimes, adaptive alleles that are beneficial elsewhere may become maladaptive if they are incompatible with local thermal or altitudinal constraints. Therefore, future research requires a multidimensional analytical framework to accurately capture the multiple drivers of latitudinal expansion. Furthermore, while recent advances in pan-genomics and global genome-wide association studies (GWAS) have identified numerous alleles associated with regional expansion in crops such as soybean, rice, and maize (Naithani et al., 2023), a significant gap remains between these theoretical discoveries and their practical application in agriculture.”

During the course of natural domestication and modern breeding, shifts in photoperiod sensitivity rarely occurred in isolation but were often accompanied by concomitant variations in associated agronomic traits. For example, in soybean, transposon insertions and structural variations in GmPHYA3 not only optimized flowering time but also conferred significant yield advantages under high-density planting at high latitudes (Qin et al., 2023). Likewise, a promoter InDel mutation in GmSTOP1a modulated photoperiod response and simultaneously enhanced tolerance to low-phosphorus conditions in low-latitude regions (Guo et al., 2026). Nevertheless, crop introduction is often accompanied by inherent physiological trade-offs. For example, expanding short-day plants into higher latitudes typically necessitates selecting for early flowering, which inherently curtails the vegetative growth phase and consequently compromises biomass accumulation and grain yield (Zhao et al., 2023a, 2023). Given these constraints, a critical imperative for future research is to leverage identified key expansion loci to accelerate regional adaptation without sacrificing established elite traits. To surmount such trade-offs, gene editing offers a promising avenue to break linkage drag. By precisely editing the coding or regulatory sequences of flanking deleterious alleles—through targeted knockouts or base substitutions—adverse effects can be eliminated without perturbing the target flowering genes. Furthermore, integrating these genetic interventions with intelligent decision support systems to dissect genotype-by-environment interactions will enable the development of breakthrough germplasms capable of achieving stable, synergistic enhancement of multiple traits across diverse agro-ecological zones. In addition, the synergy of AI-predicted genotype-environment alignments and synthetic biology-driven pathway assembly facilitates the introduction of de novo modules to drive the acquisition of superior traits.

In summary, the global expansion of crops represents more than a geographical redistribution of species; it is a broad biological process integrating environmental sensing, signal transduction, and developmental reprogramming. To confront the increasing challenges posed by extreme weather and rising food demand, modern breeding should employ advanced molecular design technologies to develop novel germplasm combining broad-spectrum environmental adaptability with high yield potential, thereby strengthening the basis for sustainable agricultural development and global food security.

Generative AI statement

The author(s) declared that generative AI was not used in the creation of this manuscript.

Any alternative text (alt text) provided alongside figures in this article has been generated by Frontiers with the support of artificial intelligence and reasonable efforts have been made to ensure accuracy, including review by the authors wherever possible. If you identify any issues, please contact us.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Footnotes

Edited by: Cheng Song, West Anhui University, China

Reviewed by: Asmamaw Menelih, Mekdela Amba University, Ethiopia

Surender Kumar, Dr. Yashwant Singh Parmar University of Horticulture and Forestry, India