The research group of Jiao Yuling in the School of Life Sciences cooperated to explain how auxin regulates leaf flattening

Flattening is a typical feature of leaves and the basis of efficient photosynthesis of plants, and its establishment mechanism is a difficult point
in developmental biology research.
Classical microdissection experiments more than 60 years ago found that leaf flattening relies on a movable signal produced by the stem tip meristem, called the Sussex signal
.
In previous studies, Professor Jiao Yuling's group from the School of Life Sciences of Peking University found that auxin polar transport at stem tips mediates Sussex signaling (Qiet al.
, 2014 PNAS), and also found that auxin signaling in leaf primordia promotes leaf margin establishment and flattening (Guan et al.
, 2017 Curr.
Biol.
）
。 However, it is unclear
how auxin polar transport at stem tips affects auxin distribution, polar gene expression, and leaf flattening within the leaf primordium.

On December 5, 2022, Jiao Yuling's research group, in collaboration with Krzysztof Wabnik, a researcher at the Polytechnic University of Madrid, Spain, published a report entitled "Polar auxin transport modulates early leaf flatterning" (DOI: 10.
1073/ pnas.
2215569119), combining experimental observations and computer simulations, revealed that auxin polar transport derived from stem tip meristem can form signal highs on both sides of the leaf primordium, activate the expression of the key gene SlLAM1 in leaf flattening at the leaf margin, and promote the establishment
of symmetrical morphology on both sides of the leaf primordium.
Previous studies in this group have shown that once the bilaterally symmetrical morphology is established, microtubule-mediated stress feedback will maintain and amplify the bilaterally symmetrical morphology to form flat and broad leaf blades (Zhao et al.
, 2020 Curr.
Biol.
）
。

Using in vivo imaging technology, this study found that blocking auxin polar transport through microsurgical cutting and drug treatment would disrupt the convergence of auxin transport protein PIN1 to both sides of the leaf primordium, reduce the level of auxin response in the leaf primordium, especially the auxin response on both sides of the leaf margin, so that DR5, which indicates auxin response, no longer appears at the leaf margin
.
Furthermore, the SlLAM1 expressed at the leaf margin shifted from leaf edge expression to adaxial surface expression in response to the change of auxin distribution (Figure 1), resulting in the leaf primordium changing from bilateral symmetry to radiation symmetry, and flattened leaves
could not be formed.
In this study, it was also observed that damage caused by surgical cutting can promote the degradation
of the adaxial polarity determinant SlREV protein.
In addition, computer model simulations predicted that the amount of auxin synthesis in early leaf primordium may affect the dependence of leaf primordium on stem auxin supply, thereby explaining why microsurgery affects leaf flattening in tomatoes and potatoes, but not in Arabidopsis
.

Figure 1.
SlLAM1 expressed at the leaf margin after microsurgical dissection was converted to nearaxial surface expression

These studies illustrate how auxin transport is involved in the flattening establishment of neo-leaf primordiums, revealing the importance of the spatial distribution of auxin signals and their temporal control of the expression pattern of the mid-lateral polar gene SlLAM1 (Figure 2).

This study deepens our understanding of
the mechanism of leaf flattening.
The degree of leaf flattening not only affects crop yield by changing the photosynthetic area, but also affects crop drought tolerance by acting on leaf transpiration
.
The understanding of the mechanism by which flattening is established will serve the molecular design breeding of crops
.

Figure 2.
Pattern diagram of polar transport-mediated auxin response and leaf developmental gene expression pattern changes

Wang Qingqing, a doctoral graduate from the Institute of Genetics and Development, Chinese Academy of Sciences, Marco Marconi, a postdoctoral fellow at the Polytechnic University of Madrid, Spain, and Guan Chunmei, an associate researcher from the Institute of Genetics and Development, Chinese Academy of Sciences, are the co-first authors of the paper, and Jiao Yuling and Krzysztof Wabnik are the co-corresponding authors
of the paper.
The research was supported
by the National Natural Science Foundation of China, the Key Research and Development Program of the Ministry of Science and Technology, and the Wang Kuancheng Education Fund.
The study is also supported by the Sino-Spanish Joint Centre for Plant and Environmental Interaction (CEPEI
).