Rishikesh Bhalerao standing in a growth room at one of UPSC's greenhouses with aspen trees in front and behind him

Bhalerao, Rishikesh P - Environmental information processing and seasonal adaptation

Research

Rishikesh Bhalerao standing in a growth room at one of UPSC's greenhouses with aspen trees in front and behind himPhoto: Andreas Palmén

Overarching goal of my research group is to understand how plants process noisy environmental information and make robust decisions that are crucial to their survival. To address this fundamental question, we are using photoperiodic and temperature regulation of the timing of growth cessation, dormancy release and bud break that are the key developmental transitions in annual growth cycle in perennial plants. We use hybrid aspen as a model system in our research.

Plants use environmental cues to make highly consequential decisions that are crucial to their survival. However environmental information such as temperature, a major regulator of plant development, is inherently noisy and how plants process such noisy information to make robust decisions remains poorly understood. Answering this fundamental question is essential to uncover mechanisms that enable plants to cope with their everchanging environment. Understanding how plants process noisy information is particularly fascinating because they make robust decisions despite lacking a central organizer such as brain in animals or a nervous system. My group is using the regulation of growth cessation, dormancy release and bud break, the key developmental transitions regulated by photoperiod and temperature to uncover molecular mechanisms that underlie environmental information processing in plants.

In long-lived trees native to boreal and temperate regions, growth stops prior to winter. The activity of shoot apical meristem (SAM) and formation and growth of leaf primordia is arrested and these are enclosed within a protective apical bud. We have identified the key components of a genetic network regulating growth cessation by photoperiod signal with sensing of shortening day length inducing growth cessation and bud break. The growth arrest is then maintained by until the advent of spring by establishment of dormancy. Dormant state is characterized by the insensitivity of SAM to growth promotive signal and involves suppression of cell-cell communication by blocking of specialized structures called plasmodesmata by callose, a polysaccharide. In order to undergo bud break and reinitiate growth in the spring, dormancy has to be broken. Release of dormancy is mediated by prolonged exposure (typical several weeks) of buds to low temperature, typically 4-8 °C. Once the buds receive sufficient chilling i. e. their chilling requirement is fulfilled, dormancy is released, progressively warmer temperatures induce bud break.

We have uncovered the key components of dormancy and bud break by temperature. A key feature of dormancy release is the restoration of cell-cell communication by deblocking of plasmodesmata by removal of callose, controlled by a recently uncovered genetic network. While these studies are highly successful, these have almost exclusively been performed in controlled growth conditions. Consequently, these studies do not reveal how buds perform long-term integration of variable (noisy) temperature signal. Our goal is to address this major gap in our understanding of mechanisms underlying variable temperature processing by trees in dormancy release and bud break in trees and from these studies provide a broader context of noisy environmental information processing in plants.

 Understanding the mechanisms underlying variable temperature processing by trees in dormancy release and bud break will provide broader insights into seasonal adaptation of trees to withstand increasingly unpredictable winter and spring temperatures caused by climate change.

Key Publications

  1. Nair A., Maurya JP., Pandey S., Singh R., Miskolczi P., Aryal A and Bhalerao RP (2025) ELF3 coordinates temperature and photoperiodic control of seasonal growth in hybrid aspen. Current Biology https://doi.org/10.1016/j.cub.2025.02.027
  2. Pandey S., Maurya JP., Aryal B., Drydna K., Nair A., Miskolczi P., Singh R., Wang X., Ma Y., Moraes T., Bayer E., Farcot E., Bassel G., Band L and Bhalerao RP (2024) A regulatory module mediating temperature control of cell-cell communication facilitates tree bud dormancy release. EMBO J: 43: 5793–5812 DOI: https://doi.org/10.1038/s44318-024-00256-5
  3. Ding J., Wang, K., Pandey S., Busov V and Bhalerao RP (2024) Molecular advances in bud dormancy in trees. Journal of Experimental Botany 75: 6063–6075 DOI: https://doi.org/10.1093/jxb/erae183
  4. Bhalerao RP (2024) Getting it right: Suppression and leveraging of noise in robust decision-making. Quantitative Plant Biology 5: e10 DOI: https://doi.org/10.1017/qpb.2024.10
  5. Azeez A., Zhao YC., Singh RK., Yordanov Y., Dash M., Misckolzi P., Stojkovic., Strauss S., Bhalerao RP* and Busov V (2021) The EARLY BUD-BREAK regulatory module in Populus. Nature Communications 12: 1123 DOI: https://doi.org/10.1038/s41467-021-21449-0 *co-corresponding author
  6. Maurya J., Misckolzi P., Mishra S., Singh R and Bhalerao RP (2020) A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen. PNAS 117(21): 11523-11530 https://doi.org/10.1073/pnas.2004705117
  7. Maurya JP., Singh R., Misckolczi P., Prasad AN., Jonsson K., Wu F and Bhalerao RP (2020) Branching regulator BRC1 mediates photoperiodic control of seasonal growth in hybrid aspen. Current Biology 30: 122-126 https://doi.org/10.1016/j.cub.2019.11.001
  8. Misckolczi P., Singh RK., Tylewicz S., Azeez A., Maurya JP., Tarkowska D., Novak O., Jonsson K and Bhalerao RP (2019) Long-range mobile signals mediate seasonal control of shoot growth. PNAS 116: 10852-10857 https://doi.org/10.1073/pnas.1902199116
  9. Singh R., Misckolczi P., Maurya JP and Bhalerao RP (2019) A tree ortholog SHORT VEGETATIVE PHASE floral repressor mediates photoperiodic control of bud dormancy. Current Biology 29: 128-133 https://doi.org/10.1016/j.cub.2018.11.006
  10. Singh R., Misckolczi P., Maurya JP., Azeez A., Tylewicz S., Busov V and Bhalerao RP (2018) A genetic network mediating the control of bud break in hybrid aspen. Nature Communications 9: 4173 https://doi.org/10.1038/s41467-018-06696-y
  11. Tylewicz S., Petterle A., Martilla S., Misckolzi P., Singh R., Immanen J., Mähler N., Hvidsten T., Eklund D., Bowman J., Helariutta Y and Bhalerao RP (2018) Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science 360: 212-215 https://doi.org/10.1126/science.aan8576

Current funding:

Logo of the Knut and Alice Wallenberg Foundation


Our work has been funded through the years by generous support from:

Logo of the Swedish Research CouncilLogo of the Knut and Alice Wallenberg FoundationLogo of the Human Frontier Science Program (HFSP)Logo of Kempestiftelserna - the Kempe FoundationsLogo of Marie Skłodowska-Curie ActionsLogo of Formas, a Swedish Research Council for Sustainable DevelopmentLogo of the Swedish Foundation for Strategic Research

 

Portrait photo of Catherine Bellini wearing a white jacket and a colourful scarf. She has short dark hair.

Bellini, Catherine - Control of Adventitious Root Initiation and Phloem Function

Research

Portrait photo of Catherine Bellini wearing a white jacket and a colourful scarf. She has short dark hair. Photo: Mattias Pettersson, Umeå University

My research focusses on two different areas using the plant model system Arabidopsis thaliana, and more recently hybrid aspen and Norway spruce. The first project which is developed at the Umeå Plant Science Center, aims at tackling the regulation of adventitious root initiation, which is a key limiting step during vegetative propagation of economically important tree species.
The second aspect, which started at the UPSC, but is now pursued in the CATS group (Carbon Allocation Transport and Signaling) headed by Dr. Sylvie Dinant at the Jean-Pierre Bourgin Institute (IJPB, from the INRAE centre in Versailles, France) focus more specifically on sugar transport and carbon allocation, and their role on plant development and interaction with the environment.

Deciphering molecular cross-talks that control adventitious root initiation

Adventitious roots (AR) are roots that develop on any organs but roots and are required for vegetative propagation of plants. Their initiation and development are limiting steps for the clonal propagation of many economically important tree species. They initiate from differentiated cells of aerial plant organs following several steps that include cell dedifferentiation, reprogramming, division and differentiation. Adventitious rooting is a quantitative genetic trait with a high phenotypic plasticity due to multiple endogenous and environmental regulatory factors. We used Arabidopsis as a model system to decipher the molecular cross-talks that control AR initiation. We have identified regulatory genes acting at several levels, including subunits of the COP9 signalosome (CSN) required for protein degradation, genes acting at the crosstalk of auxin, jasmonate and cytokinin signalling pathways. We are also interested in understanding how light signalling interacts with hormone signalling in the regulation of AR initiation. In parallel we study AR initiation in hybrid aspen, hybrid poplar and Norway spruce seedlings. In the frame of proof-of-concept projects we confirmed that the genes identified in the model system Arabidopsis, play a role in adventitious root formation in poplar cutting meaning that our basic research could lead to improvement of vegetative propagation of horticultural and forest species.

Collage of two photos showing on the left Arabidopsis seedlings from the side on a black background and on the right poplar cuttings growing in a box on transparent culture medium and pictured from below Left: Arabidopsis etiolated seedlings showing adventitious roots on the hypocotyl (adapted from Gutierrez et al 2009, Plant Cell); right: Adventitious roots on in vitro poplar cuttings (photo: Sanaria Alallaq)Schematic model showing the involved molecular components involved in adventitious root initiationTIR1/AFB2-Aux/IAA6/9/17-ARF6/8 and ARF17 signaling module is involved in the control of adventitious root initiation upstream of GH3.3, GH3.5 and GH3. (adapted from Lakehal et al. 2019; https://doi.org/10.1016/j.molp.2019.09.001)

Carbon allocation, transport and signaling (CATS team, IJPB)

In land plants, carbon allocation from the photosynthetic organs to the other organs is an integrative process enabling the plant to adjust the delivery of carbon and energetic resources depending on the plant development and environmental constraints. Thereby, carbon allocation coordinates use and storage of sugars at various scales, from the cell to the whole organism. Our goal is to determine, in the different plant organs, the mechanisms acting at a cellular, tissue and organ levels for the allocation of carbohydrates. We focus on the gene networks involved in this process and their coupling with other nutritional and developmental mechanisms, in relationship with adaptive anatomic and metabolic adjustments.

Collage of five microscope pictures of stem sections in coloured in red (left photo) and showing phloem and xylem tissues on the right photos either with lower resolution on the top and with higher resolution on the bottom. Left: Confocal image of a cross section of the basal part of the floral stem from a wild-type plant. The section was stained with blue alcian and Safranin O, and its autofluorescence was collected between 512-590 nm. (Photo: Rozenn Le Hir); right: The SWEET11-1 and SWEET12-1 genes are expressed in the phloem and the xylem tissues (Le Hir et al., 2015 Mol Plant 8, 11: 1687-1690). ph: phloem, xy: xylem.

Key Publications

  • Lakehal A, Dod A, Raneshan Z, Alallaq S, Novák O, Escamez S, Strnad M, Tuominen H and Bellini C (2020) ETHYLENE RESPONSE FACTOR 115 integrates jasmonate and cytokinin signaling machineries to repress adventitious rooting in Arabidopsis. BioRxiv 12.27.886796 - https://doi.org/10.1101/2019.12.27.886796
  • Brunoni F, Casanova-Sáez R, Šimura J, Karady M, Collani S, Ljung K* and Bellini C* (2020) Conifers exhibit a characteristic inactivation of auxin to maintain tissue homeostasis. New Phytologist. https://doi.org/10.1111/nph.16463
  • Lakehal L, Chaabouni S, Cavel E, Le Hir R, Ranjan A, Raneshan Z, Novak O, Pacurar DI, Perrone I, Jobert F, Gutierrez L, Bako L, Bellini C (2019) A molecular framework for TIR1/AFB-Aux/IAA-dependent auxin sensing controlling adventitious rooting in Arabidopsis. Molecular Plant 12 (11), 1499-1514. https://doi.org/10.1016/j.molp.2019.09.001
  • Aubry E, Dinant S, Vilaine F, Bellini C and Le Hir R (2019) Lateral transport of organic and inorganic solutes. Plants 8, 20, https://doi.org/10.3390/plants8010020.
  • Dinant S, De Marco F, Wolff N, Vilaine F, Gissot L, Aubry E, Sandt C, Bellini C and Le Hir R (2019) Synchrotron FTIR and Raman spectroscopy provide unique spectral fingerprints for Arabidopsis floral stem vascular tissues. Journal of Experimental Botany 70:871-884. https://doi.org/10.1093/jxb/ery396
  • Le Hir R, Spinner L, Klemens PAW, Chakraborti D, De Marco F, Vilaine F, Wolff N, Lemoine R, Porcheron B, Géry C, Téoulé E, Chabout S, Mouille G, Neuhaus HE, Dinant S and Bellini C (2015) Disruption of the sugar transporters AtSWEET11 and AtSWEET12 affects vascular developments and freezing tolerance in Arabidopsis. Molecular Plant 8:1687-1690. https://doi.org/10.1016/j.molp.2015.08.007

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