Seed shattering: from models to crops

Abstract

Seed shattering (or pod dehiscence, or fruit shedding) is essential for the propagation of their offspring in wild plants but is a major cause of yield loss in crops. In the dicot model species, Arabidopsis thaliana, pod dehiscence necessitates a development of the abscission zones along the pod valve margins. In monocots, such as cereals, an abscission layer in the pedicle is required for the seed shattering process. In the past decade, great advances have been made in characterizing the genetic contributors that are involved in the complex regulatory network in the establishment of abscission cell identity. We summarize the recent burgeoning progress in the field of genetic regulation of pod dehiscence and fruit shedding, focusing mainly on the model species A. thaliana with its close relatives and the fleshy fruit species tomato, as well as the genetic basis responsible for the parallel loss of seed shattering in domesticated crops. This review shows how these individual genes are co-opted in the developmental process of the tissues that guarantee seed shattering. Research into the genetic mechanism underlying seed shattering provides a premier prerequisite for the future breeding program for harvest in crops.

Keywords: domestication; domestication syndrome; fruit shedding; genetic regulation; indehiscent fruit; pod dehiscence; seed shattering.

FIGURE 1

Tissue organization and pod dehiscence process of the Arabidopsis fruit. (A) Scanning electron microscopic (SEM) micrograph of a mature silique, the different parts are indicated. (B) A close-up view of the red boxed area shown in (A), the valve, DZ, and replum are shaded with green, yellow, and blue color, respectively. (C) transversal section of the ovary region of a mature silique showing the SL has already been disintegrated and the silique opens from the replum. (D) Models for the pod dehiscence process of Arabidopsis, not to scale. The red arrows indicate the mechanical force generated in the valves. DZ, dehiscence zone; enb, endocarp b layer; LL, lignified layer; R, replum; SL, separation layer; V, valves. Scale bars in (A), 1.5 mm; (B,C), 80 μm.

FIGURE 2

The regulatory network for the differentiation of tissues that are necessary for pod dehiscence in Arabidopsis. The cartoon represents a transversal section in the mature ovary and only the replum region is shown. The different regulatory genes and tissues are indicated by distinct color in the right. The positive relationships between genes by direct evidence are shown by blue arrows and the indirect relationships are shown in dashed arrows. The negative relationships between genes are shown in red bars.

FIGURE 3

Cellular basis of seed shattering in crops. In soybeans, the loss of pod dehiscence is caused by the excessive lignification of the fiber cap cells (FCCs) and cell wall modification of the inner sclerenchyma cells in the pod valves (upper panel). The middle cartoon of the upper panel shows the transverse section of the pod ventral sutures with the yellow box shows the enlarged photo of the FCC and abscission layer. The loss of fruit shedding and seed shattering are due to the malfunction of the abscission zone (AZ) development of the pedicles (lower panel). The cartoon in the middle represents a transversal section of the AZ region as boxed in tomato, sorghum, and rice; genes with possible functional relationships that are involved in the AZ development in respective species are shown. The positive relationships between genes were shown by blue arrows. The figures and cartoons are not to scale.