Xiaoguang Shang

Genotype-to-phenotype (G2P) prediction is the central mission of modern plant breeding. Genomic data accumulation has outpaced the ability of current frameworks to predict field performance across variable environments. Statistical genomic models deliver computationally efficient breeding values but lose accuracy when applied outside training environments. Artificial intelligence (AI) extracts high-dimensional patterns at very high throughput but extrapolates unreliably under novel stress conditions. Conventional crop models encode physiological rules across environments but treat the canopy as a homogeneous layer and cannot resolve architectural variation. Functional–structural plant models simulate three-dimensional organ-level morphogenesis at the specific biological scale where genetic variation in plant architecture shapes resource capture and yield. The four paradigms address distinct layers of the G2P problem and are therefore complementary rather than substitutable. Here we propose a plant model-centred integration in which functional–structural plant models are the bidirectional hub linking upstream genomic parameter estimation, lateral multi-omics constraints, AI-based pattern recognition, and downstream canopy and field upscaling. We outline the structural rationale, review graded empirical evidence, and identify the technical conditions and benchmark trial needed to advance this framework towards operational precision breeding.

Plant cell walls are complex and dynamic cellular structures critical for plant growth, development, physiology, and adaptation. Cellulose is one of the most important components of the cell wall. However, how cellulose microfibrils deposit and assemble into crystalline cellulose remains elusive. The COBRA-LIKE plant-specific protein family plays a vital role in modulating the deposition and orientation of cellulose microfibril in plant cell walls. Here, we investigate the role of GhCOBL9 in cotton (Gossypium hirsutum) fiber development, an ideal model for studying cell elongation and cell wall thickening. The expression period of GhCOBL9 is consistent with the thickening stage of the secondary wall of cotton fibers. Overexpression of GhCOBL9 results in increased cellulose content in the cell wall and produces shorter, thicker, and stronger fibers, while RNA interference (RNAi)-mediated downregulation of GhCOBL9 leads to the opposite phenotypes, indicating its crucial role in cell wall development. Subcellular localization and binding activity assays reveal that GhCOBL9 targets the cell wall and binds to crystalline cellulose with high affinity. Transcriptomic analysis of GhCOBL9 transgenic lines uncovers expression alterations in genes related to cellulose and monosaccharide biosynthesis. Furthermore, we identify a fasciclin-like arabinogalactan protein 9 (GhFLA9) as an interacting partner of GhCOBL9 to modulate cell wall development. Additionally, the R2R3-MYB transcription factor GhMYB46-5 activates GhCOBL9 expression by binding to the MYB46-responsive cis-regulatory element in the GhCOBL9 promoter. These findings broaden our knowledge of COBL function in modulating plant cell wall development.

Cotton (Gossypium hirsutum) fiber is a highly elongated single cell with a thickened cell wall. MYB transcription factors are important regulators of plant cell elongation; however, the molecular mechanism involved in regulating fiber elongation remains to be explored. Here, we present evidence that the R2R3-MYB transcription factor GhMYB4 negatively regulates cotton fiber cell elongation by suppressing the expression of two crucial genes previously reported to affect fiber development: lipid transfer protein 4 (GhLTP4) and sucrose transporter 12 (GhSWEET12). GhMYB4 is preferentially expressed in elongating fiber cells. Knockdown of GhMYB4 in cotton results in longer fiber cells, whereas overexpression of GhMYB4 in Arabidopsis leads to reduced plant height and root length. Transcriptomic and lipidomic analyses revealed that GhMYB4 is involved in coordinating three interconnected biological processes, namely lipid content regulation, auxin signaling, and sugar metabolism. Additionally, we showed that GhMYB4 inhibits the expression of GhLTP4 and GhSWEET12 by binding to the MYB cis-element (TTTAGTG) in their respective promoters. Interestingly, bHLH transcription factor 105 (GhbHLH105) and MYB transcription factor 212 (GhMYB212) counteract the inhibitory effects of GhMYB4 on the expression of GhLTP4 and GhSWEET12, respectively. These findings provide insights into the complex molecular mechanisms regulating plant cell elongation.

Gossypium barbadense, which is one of several species of cotton, is well known for its superior fiber quality. However, the genetic basis of its high-quality fiber remains largely unexplored. Here, we resequenced 269 G. barbadense accessions. Phylogenetic structure analysis showed that the set of accessions was clustered into 3 groups: G1 and G2 mainly included modern cultivars from Xinjiang, China, and G3 was related to widely introduced accessions in different regions worldwide. A genome-wide association study of 5 fiber quality traits across multiple field environments identified a total of 512 qtls (main-effect QTLs) and 94 qtlEs (QTL-by-environment interactions) related to fiber quality, of which 292 qtls and 57 qtlEs colocated with previous studies. We extracted the genes located in these loci and performed expression comparison, local association analysis, and introgression segment identification. The results showed that high expression of hormone-related genes during fiber development, introgressions from Gossypium hirsutum, and the recombination of domesticated elite allelic variation were 3 major contributors to improve the fiber quality of G. barbadense. In total, 839 candidate genes with encoding region variations associated with elite fiber quality were mined. We confirmed that haplotype GB_D03G0092H traced to G. hirsutum introgression, with a 1-bp deletion leading to a frameshift mutation compared with GB_D03G0092B, significantly improved fiber quality. GB_D03G0092H is localized in the plasma membrane, while GB_D03G0092B is in both the nucleus and plasma membrane. Overexpression of GB_D03G0092H in Arabidopsis (Arabidopsis thaliana) significantly improved the elongation of longitudinal cells. Our study systematically reveals the genetic basis of the superior fiber quality of G. barbadense and provides elite segments and gene resources for breeding high-quality cotton cultivars.

Cell elongation is a fundamental process for plant growth and development. Studies have shown lipid metabolism plays important roles in cell elongation; however, the related functional mechanisms remain largely unknown. Here, we report that cotton (Gossypium hirsutum) LIPID TRANSFER PROTEIN4 (GhLTP4) promotes fiber cell elongation via elevating ceramides (Cers) content and activating auxin-responsive pathways. GhLTP4 was preferentially expressed in elongating fibers. Over-expression and down-regulation of GhLTP4 led to longer and shorter fiber cells, respectively. Cers were greatly enriched in GhLTP4-overexpressing lines and decreased dramatically in GhLTP4-down-regulating lines. Moreover, auxin content and transcript levels of IAA-responsive genes were significantly increased in GhLTP4-overexpressing cotton fibers. Exogenous application of Cers promoted fiber elongation, while NPA (N-1-naphthalic acid, a polar auxin transport inhibitor) counteracted the promoting effect, suggesting that IAA functions downstream of Cers in regulating fiber elongation. Furthermore, we identified a bHLH transcription factor, GhbHLH105, that binds to the E-box element in the GhLTP4 promoter region and promotes the expression of GhLTP4. Suppression of GhbHLH105 in cotton reduced the transcripts level of GhLTP4, resulting in smaller cotton bolls and decreased fiber length. These results provide insights into the complex interactions between lipids and auxin signaling pathways to promote plant cell elongation.

β-1,3-glucanase functions in plant physiological and developmental processes. However, how β-1,3-glucanase participates in cell wall development remains largely unknown. Here, we answered this question by examining the role of GhGLU18, a β-1,3-glucanase, in cotton (Gossypium hirsutum) fibers, in which the content of β-1,3-glucan changes dynamically from 10% of the cell wall mass at the onset of secondary wall deposition to < 1% at maturation. GhGLU18 was specifically expressed in cotton fiber with higher expression in late fiber elongation and secondary cell wall (SCW) synthesis stages. GhGLU18 largely localized to the cell wall and was able to hydrolyze β-1, 3-glucan in vitro. Overexpression of GhGLU18 promoted polysaccharide accumulation, cell wall reconstruction and cellulose synthesis, which led to increased fiber length and strength with thicker cell walls and shorter pitch of the fiber helix. However, GhGLU18-suppressed cotton resulted in opposite phenotypes. Additionally, GhGLU18 was directly activated by GhFSN1 (fiber secondary cell wall-related NAC1), a NAC transcription factor reported previously as the master regulator in SCW formation during fiber development. Our results demonstrate that cell wall-localized GhGLU18 promotes fiber elongation and SCW thickening by degrading callose and enhancing polysaccharide metabolism and cell wall synthesis.

Cellulose is a major component of plant cell walls and is necessary for plant morphogenesis and biomass. COBL (COBRA-Like) proteins have been shown to be key regulators in the orientation of cell expansion and cellulose crystallinity status. To clarify the role of a cotton COBL gene, GhCOBL9A, we conducted the ectopic expression and functional analysis in Arabidopsis. Previous study showed that GhCOBL9A was preferentially expressed during secondary cell wall biosynthesis in cotton fibers, and showed a significant co-expression pattern with cellulose synthase genes. Here, we detected that overexpression of GhCOBL9A induced the up-regulation of genes related to cellulose synthesis and enhanced the cellulose deposition. As a result, GhCOBL9A transgenic plants displayed increased hypocotyl and root lengths in early development, and cell wall thickening at the SCW stage. Notably, overexpression of GhCOBL9A led to an erect, robust-stature phenotype and brought higher biomass in mature plants. In addition, overexpression of GhCOBL9A in Arabidopsis AtCOBL4 mutants, a paralogous gene of GhCOBL9A, also led to a stronger growth potential, but the Atcobl4 mutant phenotype could not be rescued, implying the functional divergence of GhCOBL9A and AtCOBL4 paralogs. Taken together, these results suggest that overexpression of GhCOBL9A contributes to plant cell elongation and thickening, and increased biomass, which provides references for further utilizing GhCOBL9A to improve yield and quality traits in cotton and other species.

Cotton is an economically important crop grown for natural fiber and seed oil production. Cottonseed oil ranks third after soybean oil and colza oil in terms of edible oilseed tonnage worldwide. The fatty acid composition of cottonseed oil determines its industrial application and nutritional values. However, little progress has been made in understanding cottonseed oil biogenesis. Stearoyl-acyl carrier protein desaturase (SAD), the only known enzyme to convert saturated fatty acids into unsaturated fatty acids in plants, plays key roles in determining the fatty acid composition of cottonseed oil. In this study, we identified 9, 9, 18 and 19 SAD genes in the genomes of four sequenced cotton species: diploid Gossypium raimondii (D₅), G. arboreum (A₂), tetraploid G. hirsutum acc. TM-1 (AD₁) and G. barbadense cv. Xinhai21 (AD₂), respectively. Bioinformatic and phylogenetic analyses revealed that cotton SADs can be classified into two classes. Expression patterns showed developmental and spatial regulation of SADs in cotton. GhSAD2 and GhSAD4 were preferentially expressed in developing ovules 20–35 days post-anthesis, and significantly different expression patterns were found between high-oil and low-oil cotton cultivars, implying these two genes could be involved in cottonseed oil biogenesis. Association analysis further confirmed that GhSAD4-At expression was closely related to the oleic acid (O) content, linoleic acid (L) content and O/L value in cottonseed, implying GhSAD4 plays an important role in cottonseed oil composition. This study brings new perspectives for integrated genome-wide identification of SADs in cotton and provides references for the genetic improvement of cottonseed oil.