Pod indehiscence in common bean is associated to the fine regulation ofPvMYB26and a non-functional abscission layer

Abstract

Short title:The pod-shattering syndrome in common bean 32 33 One-sentence summary: A non-functional abscission layer determines the loss of pod 34 shattering; mapping data, and parallel gene expression and histological analysis support 35 PvMYB26 as the candidate gene for pod indehiscence.36 37The author responsible for distribution of materials integral to the findings presented in this 38 article in accordance with the policy described in the Instructions for Authors 39 (www.plantcell.org) is: Roberto Papa (r.papa@univpm.it). 40 41 42 2 43 ABSTRACT 44In legumes, pod shattering occurs when mature pods dehisce along the sutures, and detachment 45 of the valves promotes seed dispersal. In Phaseolus vulgaris, the major locus qPD5.1-Pv for pod 46 indehiscence was identified recently. We developed a BC4/F4 introgression line population and 47 narrowed the major locus down to a 22.5-kb region. Here, gene expression and a parallel 48 histological analysis of dehiscent and indehiscent pods identified an AtMYB26 orthologue as the 49 best candidate for loss of pod shattering, on a genomic region ~11 kb downstream of the highest 50 associated peak. Based on mapping and expression data, we propose early and fine up-regulation 51 of PvMYB26 in dehiscent pods. Detailed histological analysis establishes that pod indehiscence is 52 associated to the lack of a functional abscission layer in the ventral sheath, and that the key 53 anatomical modifications associated with pod shattering in common bean occur early during pod 54 development. We finally propose that loss of pod shattering in legumes resulted from histological 55 convergent evolution and that this is the result of selection at orthologous loci. 56 57 58 Keywords: pod shattering, common bean, MYB26, genome-wide association study, gene 59 expression, pod anatomy, convergent evolution, introgression lines.60 61 62 63 Loss of seed shattering is a paradigmatic example of the changes that have occurred to crop plant 64 traits compared to their wild progenitors, which collectively constitute the 'domestication 65 syndrome' (Hammer 1984). In wild species, specialised seed-dispersal strategies are of 66 fundamental importance for plant survival and fitness. Conversely, in domesticated forms, loss or 67 reduction of seed shattering is desired to reduce yield losses. 68 Due to its complex evolutionary history, common bean (Phaseolus vulgaris L.) is an 69 excellent model to study the domestication process (Bitocchi et al., 2017), which included its 70 parallel domestication in the Andes and Mesoamerica (Bitocchi et al., 2013). In P. vulgaris, the 71 dry beans are characterised by different degrees of pod shattering. These represent the majority of 72 the domesticated pool (Gepts and Debouck 1991), where a limited level of pod shattering has 73 been conserved to favour the threshing of the dry pods. Variations in the pod shattering intensity 74 are also associated with the environmental conditions during maturation (e.g., humidity and 75 temperature) (Parker et al., 2020). 76 ...

First approach to pod dehiscence in faba bean: genetic and histological analyses

“…This observation is similar to that described in Brassica species, where indehiscent species show a more lignified endocarp than dehiscent ones 54 . By contrast, our findings are opposed to those reported from histological studies in common bean and soybean, where pod valves of the wild dehiscent lines showed a strong lignified wall fiber layer contrasting with a complete absence of lignin deposition in the indehiscent lines 21 , 26 , 34 , 55 , 56 , 58 .…”

“…Histological characterization of the faba bean pod sutures in mature pods revealed anatomical structures analogous to those described in other legumes such as soybean, common bean, pea or common vetch 22 , 26 , 30 , 36 , 55 , 56 . Pod dehiscence arises from fissures that initiate in the ventral sutures, as recently observed in chickpea by Aguilar-Benitez 28 .…”

“…Thus, although the cell walls in the sheath were heavily thickened in both parental lines, the cell lumen appeared to be almost occluded in the indehiscent Vf6 compared to the primitive dehiscent line Vf27. A major lignification in the DZ was reported to confer dehiscence resistance to mature pods in soybean 22 , Brassica napus 54 and P. vulgaris 26 , 55 , 56 . Moreover, observation of the anatomical structure of pod ventral sutures in common vetch ( V. sativa ) revealed that all dehiscent vetches have abscission layers in the DZ that are absent in the indehiscent plants 57 .…”

Same Locus for Non-shattering Seed Pod in Two Independently Domesticated Legumes, Vigna angularis and Vigna unguiculata

“…On the other hand, MYB26 is expressed in seed pods in many legume species according to the expression database [ Vig GS, the Phaseolus vulgaris Gene Expression Atlas ( Pv GEA) 8 and Soybean eFP Browser 9 ]. In addition, Di Vittori et al (2020) has recently revealed in common bean that reduced expression of MYB26 is a key for non-shattering genotypes. Thus, in legumes, MYB26 plays a crucial role in the development of pod sclerenchyma and has been a common target of human selection among the three independently domesticated legumes, azuki bean, cowpea, and common bean.…”

Toward the introgression of PvPdh1 for increased resistance to pod shattering in common bean

“…A recently discovered QTL on Pv05, in immediate vicinity of PvMYB26, is associated with a loss of dehiscence in the Andean gene pool (Rau et al 2019;Parker et al 2020;Di Vittori et al 2020). This locus was mapped in detail in a biparental recombinant inbred population (Rau et al 2019), which also found signiicant QTLs on Pv04 and Pv09 in the same population.…”