Deciphering spike architecture formation towards yield improvement in wheat

The domestication of wild species into cultivated crops was the driving force for the Neolithic revolution that transitioned nomadic humans from hunter-gatherers to agricultural societies more than 10,000 years ago (Doebley et al., 2006). All domesticated crops share a set of characteristics known as the 'domestication syndrome' (Hammer, 1984), which include larger and more numerous fruits or seeds, robust plants, reduced dispersal losses, loss of seed dormancy, and reduced bitterness or toxicity. Wheat was one of the first domesticated crops, and this domestication was mainly determined by two genes, brittle rachis (Br) and Q (also named AP2L5). Br determines the non-shattering ability of seeds, while Q/AP2L5 affects the free-threshing trait (Simons et al., 2006; Avni et al., 2017). Additionally, increasing yields was the primary goal of crop domestication and breeding, and inflorescence architecture largely determined grain productivity. As a result, spike architecture is one of the most important targets of wheat domestication and breeding.

Different crops possess varied inflorescence morphology. Inflorescence in wheat is an unbranched and determinate compound spike, consisting of multiple sessile spikelets borne in two staggered rows on the spike axis; each of spikelet generally forms 4-6 fertile florets (Shitsukawa et al., 2009). Rice develops a panicle that produces indeterminate primary and secondary branches with one fertile floret spikelet (Gao et al., 2019). By contrast, wheat branches degenerate and the main rachis produces spikelets directly, so fewer spikelets are formed but more florets are produced. Unbranched barley (Hordeum vulgare) produces spikelet triplets on the rachis (consisting of a central spikelet and two lateral spikelets), each of which contains a single floret (Koppolu and Schnurbusch, 2019).

Domestication and breeding selection have driven crops to undergo important inflorescence morphological changes, which are generally associated with spikelet number and spatial arrangement, as well as floret fertility (Faris, 2014). In rice, the elite allele of SOUAMOSA PROMOTER BINDING PROTEIN-LIKE 14 (OsSPL14), also known as Ideal Plant Architecture 1 (IPA1), increases branching and grain numbers to improve yield (Jiao et al., 2010; Miura et al., 2010). Via introgression of the OsSPL14WFP allele into elite indica cultivars, International Rice Research Institute (IRRI) has bred five high-yielding rice varieties (Kim et al., 2018). Additionally, elite ipa1-1D alleles have been introduced into Chinese main planting varieties via marker assisted selection (MAS), generating the novel cultivar “Jia you Zhong ke” with improved yield performance (Wang et al., 2018a). CRISPR-Cas9-mediated mutation of dense and erect panicle 1 (OsDEP1), an important regulatory gene for shaping spike architecture, has been used in rice breeding for producing more florets per panicle (Li et al., 2016). In maize, ZmCLAVATA3/EMBRYO SURROUNDING REGION-RELATED7 (ZmCLE7) and ZmFON2-LIKE CLE PROTEIN1 (ZmFCP1) weak alleles increase kernel row number and grain yield, which are beneficial for maize high yield breeding (Chen and Gallavotti, 2021; Liu et al., 2021b). Allelic variation in Vulgare Six-rowed spike 1 (Vrs1), which contributes to higher grain number in barley, is a driving force of inflorescence morphology and had a significant effect on row-type during barley domestication (Sakuma and Schnurbusch, 2020). Thus, a number of genes that regulate inflorescence architecture have been identified and modulated in elite crop variety breeding in rice, maize, and barley. However, gene cloning and functional studies in wheat spike architecture regulation and breeding application have lagged behind other crops partially due to the complexity of the wheat genome.

Currently, several strategies commonly used to identify factors for wheat spike development include homologous cloning by comparison with known factors in Arabidopsis thaliana and rice, and positional cloning by linkage mapping or genome-wide association studies (GWAS) (Li et al., 2019b; Yu et al., 2019; Li et al., 2020a). As well, TILLING mutants are helpful in identifying spike morphology-related genes and characterizing their functions (Zhang et al., 2021). The strategy of gene cloning and molecular mechanism dissecting of wheat spike development has been significantly improved due to the continuous release of wheat reference genomes (IWGSC, 2014, 2018; Sato et al., 2021; Shi et al., 2022), the collection of large numbers of germplasm resources (landraces and Triticeae relatives) (Guo et al., 2020; Hao et al., 2020), the establishment of mutant libraries (Krasileva et al., 2017; Wang et al., 2022a), the construction of high-throughput phenotyping platforms (Furbank and Tester, 2011; Chen et al., 2014), and the development of new genome editing tools and improved genetic transformation efficiency in wheat (Wang et al., 2018a; Liu et al., 2022; Wang et al., 2022b). These emergent resources and tools will accelerate the isolation of genes underpinning spike morphogenesis and concomitant yield grain.

In this review, we summarize the genetic regulatory pathways for determination of spike formation and the technology roadmaps for gene cloning and functional study, as well as highlight the current breeding applications in wheat. Furthermore, we speculate on the development of genetic manipulation and precision design of spike architecture for future wheat breeding.

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