Abstract
A fundamental feature of sexual reproduction in plants and animals is the specification of reproductive cells that conduct meiosis to form gametes, and the associated somatic cells that provide nutrition and developmental cues to ensure successful gamete production. The anther, which is the male reproductive organ in seed plants, produces reproductive microsporocytes (pollen mother cells) and surrounding somatic cells. The microsporocytes yield pollen via meiosis, and the somatic cells, particularly the tapetum, are required for the normal development of pollen. It is not known how the reproductive cells affect the differentiation of these somatic cells, and vice versa. Here, we use molecular genetics, cell biological, and biochemical approaches to demonstrate that TPD1 (TAPETUM DETERMINANT1) is a small secreted cysteine-rich protein ligand that interacts with the LRR (Leucine-Rich Repeat) domain of the EMS1 (EXCESS MICROSPOROCYTES1) receptor kinase at two sites. Analyses of the expressions and localizations of TPD1 and EMS1, ectopic expression of TPD1, experimental missorting of TPD1, and ablation of microsporocytes yielded results suggesting that the precursors of microsporocyte/microsporocyte-derived TPD1 and pre-tapetal-cell-localized EMS1 initially promote the periclinal division of secondary parietal cells and then determine one of the two daughter cells as a functional tapetal cell. Our results also indicate that tapetal cells suppress microsporocyte proliferation. Collectively, our findings show that tapetal cell differentiation requires reproductive-cell-secreted TPD1, illuminating a novel mechanism whereby signals from reproductive cells determine somatic cell fate in plant sexual reproduction.
Highlights
Successful sexual reproduction depends on the specification of different types of somatic and reproductive cells that give rise to eggs and sperm in both plants and animals
The anther produces reproductive microsporocytes that give rise to pollen, as well as surrounding somatic cells that support the normal development of pollen
We demonstrate that TPD1 (TAPETUM DETERMINANT1) is processed into a small secreted cysteine-rich protein ligand for the EMS1 (EXCESS MICROSPOROCYTES1) leucine-rich repeat receptor-like kinase (LRR-RLK)
Summary
Successful sexual reproduction depends on the specification of different types of somatic and reproductive cells that give rise to eggs and sperm in both plants and animals. The central reproductive microsporocytes (or pollen mother cells) are surrounded by four concentrically organized somatic cell layers: the epidermis, endothecium, middle layer, and tapetum (listed from outside to inside). The subepidermal L2 cells differentiate into primary parietal cells (PPC), which undergo periclinal division to produce two layers of secondary parietal cells (SPC). The outer SPC (OSPC) form the endothecium adjacent to the epidermis, and the inner SPC (ISPC) undergo a further periclinal division to establish the middle layer and tapetum, which completes the cell fate specification events in the anther lobe. As the anther is centrally important for plant sexual reproduction and breeding, it is imperative that we obtain an in-depth understanding of the molecular mechanisms underlying somatic and reproductive cell differentiation during anther development
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